Floristic and ecological attributes of a Seasonal Semideciduous Atlantic Forest in a key area for conservation of the Zona da Mata region of Minas Gerais State, Brazil1

(Floristic and ecological attributes of a Seasonal Semideciduous Atlantic Forest in a key area for conservation of the Zona da Mata region of Minas Gerais State, Brazil). We evaluated the floristic and ecological attributes of a seasonal semideciduous forest remnant (SSF) (500-1,050 m) located in a key area for biodiversity conservation. The importance of the fragment to the ecosystem conservation was revealed by its species richness (253), diversity (Shannon index = 4.6; Simpson’s complementary index = 0.98) and evenness (Pielou index = 0.83), which are considered high values for a SSF. Zoochory occurred in 77% of the species, indicating the existence of important biotic interactions that ensure the occurrence of gene flow. We recorded 14 endangered species, among which two are rare (Trigynaea oblongifolia and Trattinnickia ferruginea) and two are indicators of mature forests (Trattinnickia ferruginea and Virola bicuhyba). We confirmed the importance of key areas for biodiversity conservation and of the Atlantic SSF located at the 0-1,000 m altitudinal range. These areas deserve attention from conservationists due to the high species richness and high number of endemic and endangered species.


Introduction
Key areas for biodiversity conservation are sites of high value on a global scale (Giulietti et al. 2009).
Such key areas are geographic units large enough to maintain viable populations and can be identified by criteria based on species vulnerability and endemism (Langhammer et al. 2007, Giulietti et al. 2009).In Brazil, the analysis of the occupation of key areas for biodiversity conservation reveals a predominance of these areas in the Atlantic Forest (Giulietti et al. 2009).
The Atlantic Forest is one of the 35 biodiversity hotspots in the world (Zachos & Habel 2011).More than 80% of its remnants have less than 50 ha; such remnants are damaged by border effect and by the distance between fragments (Ribeiro et al. 2009).These small fragments are also among the priorities for conservation of the Atlantic Forest and as such must be properly managed to keep the functional link among the vegetation mosaics, minimize border effect and improve connectivity between fragments (Ribeiro et al. 2009).
Connectivity between fragments aims to aid individual and gene flow among populations and subpopulations and to increase their chances of survival, thus enabling the maintenance of ecological and evolutionary processes on a large scale (Ayres et al. 2005).Management of connectivity between fragments has been made by means of ecological corridors.The Central Corridor of the Atlantic Forest, for instance, currently encompasses 11 areas of high priority for conservation of the region and possesses the highest vascular plant diversity in the world (Ayres et al. 2005).
The Parque Nacional do Caparaó, located between Minas Gerais and Espírito Santo States, Brazil, integrates the Central Corridor of the Atlantic Forest.Furthermore, that park, along with the Parque Estadual da Serra do Brigadeiro and their respective surrounding forest fragments, form a key area for biodiversity conservation (Giulietti et al. 2009).We aimed to study issues of floristic, ecological, and conservationist interest in a forest remnant between those two Protected Areas, by addressing the following questions: 1) What are the tree species composition and diversity in the area?2) Which is the predominant seed dispersal syndrome in the area?3) Are there endemic tree species in the studied fragment?4) Which and how many tree species are threatened with extinction on a statewide (Red List of Plant Species Threatened with Extinction in Minas Gerais State; Biodiversitas 2008), nationwide (Martinelli & Moraes 2013), and worldwide scale (Red List of Threatened Species of the International Union for Conservation of Nature -IUCN)?5) Which and how many species are classified as rare, following Giulietti et al. (2009) and Martinelli & Moraes (2013)?While answering these questions, we also aimed to address their implications on biodiversity conservation.

Material and methods
The study area consists in a Montane Seasonal Semideciduous Forest remnant in the Zona da Mata region of Minas Gerais State, Brazil, located in the surroundings of the Central Corridor of the Atlantic Forest, between Parque Nacional do Caparaó and Parque Estadual da Serra do Brigadeiro (figure 1).The region is considered key for the conservation of rare species (Giulietti et al. 2009).
The studied forest remnant is located within the private property Santa Rita Farm (20°46'S, 42°02'W), at Faria Lemos municipality, on the watershed of Paraíba do Sul river.The fragment extends throughout an area of ca.219 ha, with altitudes ranging between 500 and 1,050 m.The history of occupation of the site reveals areas with different land uses: recovering areas, which were deforested in the 1960s and 1970s for coffee cultivation and wood exploitation; and predominantly well-preserved forest patches that did not undergo significant anthropic action.Koppen's climate in the region is Tropical Aw, characterized by high temperatures, with an annual mean of 24.5 ºC (Peel et al. 2007).Mean annual precipitation is 1,200 mm, with high values being registered in the rainy season, which takes place from October through April.
For vegetation sampling, we established three transects 20 m wide and 400 m long each, parallel and distant 200 m from one another.In each transect we established 11 400-m 2 plots (20 × 20 m), totaling 33 plots and 1.32 ha of sampling area.Plots were placed in order to be equidistant 20 m from one another along transects.Then, we sampled all tree individuals having circumference at 1.30 m above ground level equal to or higher than 15 cm.Individuals with tillers below the 1.30-m mark above ground level had all their bifurcations included in the sampling whenever at least one of the tillers met the sampling criterion.Then, we measured the perimeter of each of the other bifurcations separately and calculated their respective basal areas; only then we calculated the sum of the basal area of tillers (Moro & Martins 2011).Botanical material was identified by consultation to herbaria Guido Frederico João Pabst (GFJP) and Herbário do Jardim Botânico do Rio de Janeiro (RB), review of specialized literature, and by sending duplicates to specialists.Species were grouped in families following the classification system APG III (2009) and species' authors were checked in the online platforms Missouri Botanical Garden (http://www.mobot.org/)and Flora do Brasil (http://floradobrasil.jbrj.gov.br/).All collected botanical material was deposited in the GFJP herbarium, in Carangola city, Minas Gerais State.
Species distribution was investigated based on two endemism criteria: (i) endemic to Brazil, and (ii) endemic to the Atlantic Forest.From this stage, we used only specimens identified at the species level in order to obtain higher data reliability in our analyses.To access such endemism criteria, we consulted databases Flora do Brasil (http://floradobrasil.jbrj.gov.br/) and SpeciesLink (http://splink.cria.org.br/), and the following literature: Catálogo das Árvores Nativas de Minas Gerais (Oliveira-Filho 2006), Plantas da Floresta Atlântica (Stehmann et al. 2009), and Árvores da Floresta Estacional Semidecidual -Guia de Identificação de Espécies (Ramos et al. 2008).Ecological representativeness of species was evaluated by their dispersal syndrome, which is an important attribute to characterize environments and can be measured by the amount of plants that have zoochoric or the different abiotic syndromes (Campassi 2006).In that sense, we classified syndromes under categories zoochoric or abiotic based on diaspore morphology and on the review of literature on fruit and seed dispersal (e.g., van der Pijl 1982, Morellato et al. 2000, Catharino et al. 2006, Kinoshita et al. 2006, Campassi 2006, Yamamoto et al. 2007, Aquino & Barbosa 2009, Prado-Júnior et al. 2012).
The degree of threat to the sampled species was evaluated by consultation to the IUCN Red List of Threatened Species (http://www.iucnredlist.org/),Livro Vermelho da Flora do Brasil (Martinelli & Moraes 2013), and Lista Vermelha das Espécies da Flora Ameaçada de Extinção em Minas Gerais (Biodiversitas 2008).The rarity status of species was determined following Giulietti et al. (2009) and Martinelli & Moraes (2013).
Fabaceae, Rubiaceae, and Myrtaceae are among the 10 most representative botanical families in the Brazilian flora (BFG 2015).These families are also among the richest ones in terms of species and endemism in the Atlantic Forest (Stehmann et al. 2009).
Fabaceae genera that show high richness in the Atlantic Forest were found in the study area, such as Inga Mill.and Machaerium Pers.(Stehmann et al. 2009).According to Oliveira-Filho & Fontes (2000), the abovementioned genera are the most important ones in the Fabaceae that occur in seasonal forests, which is the case of the forest remnant we studied.
The most representative genera in the study area were Ocotea Aubl., with seven species; Eugenia L., Myrcia DC. and Licania Aubl., with five species, each; and Aspidosperma Mart., Cupania L., and Trichilia P. Browne, with four species, each.Ocotea is the most species-rich genus of Lauraceae in Brazil, while Eugenia and Myrcia are the most diverse Myrtaceae genera (BFG 2015) and are among the 20 most diverse genera in the Atlantic Forest (Stehmann et al. 2009).
Other less diverse genera found, yet that are represented among the richest ones in the Brazilian  (Stehmann et al. 2009).Species diversity in the study area was 4.6 according to Shannon-Wiener's index (H') and 0.98 according to Simpson's complementary index (1-D).Pielou's evenness (J') was 0.83.Meira-Neto & Martins (2000) established maximum and minimum values for Shannon (H' between 3.2 and 4.2) and evenness (J' between 0.73 and 0.88) indexes to the Zona da Mata region of Minas Gerais State.Our data thus yielded results above those marks.In comparison with studies performed in other seasonal semideciduous forest remnants that used similar sampling methods (e.g., Silva et al. 2004, Marangon et al. 2007, Leite & Rodrigues 2008, Dias-Neto et al. 2009, Braga et al. 2011, Santos et al. 2013, Coelho et al. 2016), the values of richness, diversity, and evenness found at Santa Rita Farm were also higher.The high values of those indexes found in our study provide evidence of the ecological importance of the studied fragment, which is located between two important Protected Areas (PAs) of the Atlantic Forest, namely the Parque Estadual da Serra do Brigadeiro and the Parque Nacional do Caparaó.In that sense, should an ecological corridor be implemented between those PAs, the remnant might well represent a strategic area for the maintenance of gene flow in the region.A total 140 specimens were identified at the species level.Regarding their distribution in Brazil, 77 species (55%) are not endemic and 62 (44%) are endemic to the country.This latter value reflects the pattern overall found in the Brazilian flora, which has a high degree of endemism of seed plants -57.4% of all phanerogams occurring in Brazil (BFG 2015).Psidium guajava L. was the only non-native species registered in our study (Sobral et al. 2016) while Ixora brevifolia Benth was the only species whose distribution is currently unknown (Di Maio 2016).
We registered 44 species endemic to the Atlantic Forest (31%) (table 1).The Atlantic Forest is known by its high endemism (Myers et al. 2000;Ribeiro et al. 2011).However, the percentage of endemic species in this hotspot has slightly decreased from 50.2% in 2010 to 49.5% in 201549.5% in (BFG 2015)).Such reduction in the percentage of endemism can be justified by the increase in knowledge on the distribution of species and by the area of Atlantic Forest inserted in other vegetation domains, like the gallery forests in the Cerrado and the enclaves in the Caatinga (BFG 2015).
The most representative dispersal syndrome was zoochory, which was found in 108 species (77%).The abiotic dispersal syndrome, on the other hand, was found in 32 species, which represent 23% of all sampled species (table 1).Our results are in line with the pattern found in the Atlantic Rainforest, in which, analogously to other tropical forests (Fleming 1979, Jordano 2000), zoochory is the predominant syndrome (Campassi 2006).Such pattern found in tropical forests is related to the absence of long seasonal periods (e.g., Morellato et al. 2000).In other words, rates of zoochorous dispersal decrease with increasing rainfall seasonality.
Forest fragmentation, fruit collection by humans, and long-term defaunation are the major factors responsible for the loss of interaction between dispersers and dispersed species (Fuentes 2000).Evidence that defaunation, especially of large frugivorous species, can lead to the disappearance of plant species with large seeds that significantly contribute to the maintenance of carbon stock in the Atlantic Forest has been reported (Bello et al. 2015).
In that sense, it is worth noting that the studied remnant plays an important ecological role in the region, as it provides food to local fauna.However, performing a floristic survey and implementing management practices for conservation of animal species in the region are essential to maintain the more than 70% of angiosperm species therein.
A total 14 threatened species were recorded in our survey (table 2).The main threat to populations of Aspidosperma polyneuron Müll.Arg., Apuleia leiocarpa (Vogel) J.F. Macbr., Cedrela fissilis Vell., Dalbergia nigra (Vell.)Allemão ex Benth., Joannesia princeps Vell., Melanoxylon brauna Schott, and Zeyheria tuberculosa (Vell.)Bureau ex Verl. is related to predatory exploitation by the timber industry and rural producers for manufacture of laminate and solid wood furniture as well as of ornamental structures, all of which have been historically leading to population decline in those species (Biodiversitas 2008, Martinelli & Moraes 2013, IUCN 2016).Trigynaea oblongifolia Schltdl. is considered rare (Martinelli & Moraes 2013), and similarly to Brosimum glaziovii Taub.(IUCN 2016), the species has a restricted distribution, which is the major threatening factor to both species.Populations of T. oblongifolia are threatened by loss of habitat quality (Martinelli & Moraes 2013).Euterpe edulis Mart. is threatened by its intense exploitation for palm heart harvest across the entire area where it occurs and by the consequent decline of its populations.Trattinnickia ferruginea Kuhlm. is a rare species (Giulietti et al. 2009), with populations restricted to well preserved Atlantic Forest remnants in Minas Gerais State; additionally, it is threatened by loss of its occurrence area and of habitat quality due to deforestation for charcoal production, pastures, and silviculture.Cariniana legalis (Mart.)Kuntze populations are declining not only due to intense exploitation for wood extraction, but also due to their occurrence in fertile lands widely used in agriculture.Virola bicuhyba (Schott) Warb. is endemic to ombrophilous and semideciduous Atlantic Forests and occurs preferentially in areas at advanced stages of regeneration or at climax (Martinelli & Moraes 2013).V. bicuhyba has medicinal value and its wood has high economic importance.Its major threat is the reduction of its populations, which is mainly caused by selective extraction and habitat conversion (Martinelli & Moraes 2013).
Besides the rare and threatened species recorded in our survey, the studied fragment has also other species classified under those categories, like Mascagnia velutina C.E. Anderson, which is rare (Giulietti et al. 2009) and is considered vulnerable due to high fragmentation of five among ten localities of its occurrence (Biodiversitas 2008), and Sinningia carangolensis Chautems, which is a rare species restricted to the region of Carangola municipality, Minas Gerais State, and is thus considered endangered

Figure 1 .
Figure 1.Geographic location of the Seasonal Semideciduous Atlantic Forest fragment at Santa Rita Farm, Faria Lemos municipality, Minas Gerais State, Brazil.Key areas for conservation of rare plants, Parque Estadual da Serra do Brigadeiro, Parque Nacional do Caparaó, Santa Rita Farm, Faria Lemos, Minas Gerais State, Brazil.