Phanerogamic flora and vegetation of Itacolomi State Park , Minas Gerais , Brazil

Located in the municipalities of Ouro Preto and Mariana, in the Quadrilátero Ferrífero (QF) of Minas Gerais, the Itacolomi State Park (ISP) shelters more than 7,000 ha of remnants of Atlantic Forest and campos rupestres. The QF region has high biodiversity and is being highly impacted, mainly by mining activities. Aiming to organize the available floristic information and to support related research, this study presents the list of phanerogamic species of the ISP and the major vegetation types. This survey was carried out from October/1992 to July/2006, by monthly field trips. Besides authors ́ personal collections, other records were assembled from herbarium databank. A total of 1623 taxons belonging to 122 families were listed. The families with higher species richness were Asteraceae, Fabaceae, Melastomataceae, Poaceae and Orchidaceae. The vegetation is represented by campos rupestres (51% of the total area), followed by montane forests (40%) and anthropogenic disturbed areas (9%). The greatest species richness occurs in campos rupestres. Several species are threatened and/or endemic. The knowledge of phanerogamic flora of ISP can help the Management Plan of this Unit of Conservation. It is also a contribution for future-related studies of the flora of ISP, Minas Gerais and Brazil.


Introduction
Minas Gerais is the Brazilian State with the highest richness and endemism of Angiosperm species and harbors important phytogeographical domains (BFG 2015).Among them, the Atlantic Forest and the Cerrado are the largest, richest and more threatened ones (Fundação SOS Mata Atlântica 1998, Coutinho 2006).Atlantic Forest is one of the most biologically rich and diverse domain in the world, with around 20,000 plant species, representing 8% of the Earth's flora (Fundação SOS Mata Atlântica 1998).In spite of the Atlantic Forest being considered a biodiversity hotspot (Myers et al. 2000), it was reduced to less than 12% of its original size, with most of the remaining areas restricted to Conservation Units (Ribeiro et al. 2009).
With regard to Brazilian vegetation, the campos rupestres stand out due to the peculiar and rich biodiversity.They occur from an altitude of 900m above sea level and upwards, mainly along the Espinhaço Range, in the States of Minas Gerais and Bahia, and with disjunct parts of the same chain, between latitudinal limits of 21º10' and 10º S (Giulietti & Pirani 1988).Phytogeographically, the campos rupestres are classified into the Cerrado domain (Coutinho 2006, Batalha 2011), a kind of savanna, where plants grow in a wide variety of substrates including rock outcrops of quartzite, sandstone or ironstone, along with sandy, stony and waterlogged grasslands (Silveira et al. 2016).Campos rupestres also harbor several endemic and threatened species from different groups of organisms (Echternacht et al. 2011, BGF 2015, Silveira et al. 2016).Among the 538 threatened plant species of the Minas Gerais State, 358 (66.5 percent) occur in this kind of physiognomy (Costa et al. 1998).Among the Brazilian vegetation types, the campos rupestres have the highest percentage of endemism (1,951 endemic out of 4,928 species) (BGF 2015) The Quadrilátero Ferrífero (Iron Quadrangle) Region (QF) covers an area of 7,000 km 2 , in the central portion of the Minas Gerais State (Dorr 1969).This region is considered to be of extreme biological importance (Costa et al. 1998).The QF landscape is a mosaic under the influence of two Brazilian hotspots, Cerrado and Atlantic Forest, giving evidence of the ecotonal character of the region (Echternacht et al. 2011).The Atlantic Forest in the QF Region is mainly represented by a seasonal semideciduous type (Morellato & Haddad 2000) and the Cerrado occurs in different phytophysiognomies, including the campos rupestres (Silveira et al. 2016).The campos rupestres in the Quadrilátero Ferrífero, occur frequently in areas with quartzite rocks, interspersed mainly with banded iron formation (BIF´s), also known as cangas (Messias et al. 2011(Messias et al. , 2012(Messias et al. , 2013)).Cangas are one of the most diverse, threatened and least studied ecosystems of southeast Brazil (Jacobi et al. 2007).In spite of the great biodiversity, mining, as well as metallurgical industries, urban expansion, among other activities, have provoked a high environmental impact in the Quadrilátero Ferrífero Region (Jacobi et al. 2007).
Itacolomi State Park is one of the few full protection conservation units in this region (IEF 2016) and shelters more than 7,000 ha of remnants of Atlantic Forest and campos rupestres.Most of the campos rupestres are quartzitic, but ISP is one of the three full protection parks of Minas Gerais also harboring ferruginous campos rupestres.Thus, this conservation unit in this region plays an important role in protecting biodiversity.
Little is still known about Itacolomi State Park flora, whose domain is an ecotone region between the Atlantic Forest and the Cerrado.There were found only a preliminary checklist of campos rupestres (Peron 1989), specific family studies about Orchidaceae (Alves 1990, Batista et al. 2004), Leguminosae (Dutra et al. 2005, 2008a, 2008b, 2009, 2014, Lima et al. 2007, 2010), Bromeliaceae (Coser et al. 2010), Myrtaceae (Bünger et al. 2012) and Asteraceae (Barnadesieae e Mutiseae) (Almeida et al. 2014).And also, few floristic studies have been recently published on small patches of campos rupestres (Gastauer et al. 2012) and forests (Pedreira & Sousa 2011) of this conservation unit.The aims of this study are to present a brief description of the vegetation of Itacolomi State Park (ISP) and to present a checklist of the phanerogamic flora.According to Peron (1989) the vegetation at ISP is formed mainly by campos rupestres permeated by riparian or semideciduous forest fragments.
The climate, according Köppen classification is Cwb, i. e. mesotermic, with a warm and rainy season from September to April with a dry season from May to August (Álvares et al. 2013).The annual mean rainfall is 1,250 mm and the annual mean temperature is about 20°C (varying from 4 to 33ºC).Fog is frequent, especially during the dry season.
The relief is characterized by steep slopes where the altitudes varies from 700 to 1772 m.The Park covers the greatest part of Itacolomi Hill, at the southern of Espinhaço Range, with around 7,500 ha (Castañeda 1993).The geology of ISP comprises clastic metasedimentary rocks from Rio das Velhas and Minas Supergroups, Sabará and Itacolomi Groups.The quartzite of Itacolomi Group occurs in the greatest proportion of the Park area.There are also intrusions of metabasic rocks and a superficial iron crusts known as canga (Castañeda 1993).According to the same author, the soils at Itacolomi vary from sandy shallow soils, mostly associated to quartzite, occurring in campos rupestres to deeper ones, mainly Latossols (Oxisols), at forest patches at lower altitudes.
This survey was carried out from October/1992 to July/2006, when monthly field trips were taken, all over the Park.The collected species were herborized and deposited in the Professor José Badini Herbarium (OUPR) at Federal University of Ouro Preto.The species identification was made by comparison with previously identified material at RB, BHCB, VIC and OUPR herbaria, by using specialized literature and with the help of specialists.
Aiming to supplement the checklist, records from SpeciesLink (CRIA 2016) and JABOT (JBRJ 2016) databank were included.Materials determined only at the family level were not considered and the ones identified at generic level were included only when deposited in OUPR and assumed they were different from the species already listed.Records included in the checklist appear cited with acronyms according to Thiers (2016).
The circumscription of families followed the Angiosperm Phylogeny Group -APG III (Chase & Reveal 2009).The species names were checked with the database of the list of species of the Brazilian Flora 2020 Project (2016) and The Plant List (2013).Each species was described by its habit (Rizzini 1997) and habitat.The forest vegetation was classified according to Veloso et al. (1991) and the grasslands areas followed Ferri (1980), Eiten (1983) and Giulietti et al. (1987).The major vegetation types are Montane Forest (F), Campos Rupestres (CR) and Anthropogenic Disturbed Areas (AA).In order to recognize the threatened species, it was consulted the IUCN Red List (2015), as well as the Brazilian (MMA 2014) and Minas Gerais (COPAM 1997) Red Lists.
The vegetation map was made using an IKONOS image, which was provided by the State Forest Institute of Minas Gerais (IEF).The vegetation groups described were identified in the field campaigns and then designed in Geographic Information System (GIS) environment with Arcview 9.2 software (Environmental Systems Research Institute, 2007).

Results and Discussion
A total of 1614 species, one subspecies and eight varieties, belonging to 569 genera and 122 families were identified (Table 1).The species richness in ISP is comparable with other mountainous areas along the Espinhaço Range, e.g.Pico das Almas: 930 species (Stannard et al. 1995), Ibitipoca: 1080 species (Forzza et al. 2013), Grão Mogol: 1073 species (Pirani et al. 2003), Serra de São José: 1087 species (Alves & Kolbek 2009) and Serra do Cipó: 1530 species (Giulietti et al. 1987).These results highlight how diverse is the ISP flora as well as the importance of focusing on further taxonomic studies in this park.diversity, wide latitudinal and altitudinal range, isolation and influence of different vegetation domains (Giulietti et al. 1997, Jacobi et al. 2007, Silveira et al. 2016).
The subshrubs represented 30% of the species, followed by shrubs (25%), herbs (19%), trees (13%), lianas (12%) and few palms and epiphytes (Figure 5).Shrubby species occur in both forest and campos rupestres, explaining the higher richness of this habit.In addition, the southern portion of the Espinhaço Range is more strongly influenced by the Atlantic Forest than the central/northern parts, leading to a higher proportion of phanerophytic species in campos rupestres (Echternacht et al. 2011).Most of the herbs occur in campos rupestres, mainly from Poaceae and Orchidaceae families.The epiphytes seem to be sub sampled since the montane forests of the region are reported as having a greater richness of this life-form (Ferreira, 2011).Some parts of the forest are mono-dominated by Eremanthus erythropappus, known locally as candeal, similar to the other areas of Espinhaço Range (Oliveira-Filho & Fluminhan-Filho 1999, Kamino et al. 2008).Most of these areas are in primary succession after fire occurrence.
The environmental impact in the ISP region dates back to the early seventeenth century, with gold mining.Later, with the decline of gold rupestres occur in the highest parts of the ISP, always higher than 1000m, and the forests mostly in the lower ones, from 700m to 1300m, usually along streams and slopes with deeper soil.
The forests at Itacolomi State Park have the same pattern of the forests along the Espinhaço Range (Harley 1995), varying considerably both in composition and structure in response to the geo-climatic conditions, often resulting in a large heterogeneity of patterns, even in a relatively small area.Thus, as described by Kamino et al. (2008), a riparian forest on the valleys may be evergreen, while the adjacent forest on the slope is semideciduous.In fact, Pedreira & Sousa (2011) described a swampy evergreen forest patch in Itacolomi State Park, surrounded by semideciduous forests, with well-drained soils.In spite of the existence of this small scale variation in Itacolomi State Park forest fragments, they were only characterized in this work by the general feature as "montane forest".
Forest ecosystems with striking seasonality of rainfall or low soil water retention often drive high proportions of deciduous and semideciduous species in their communities (Reich & Borchet 1984, Lenza & Klink 2006).However, the fog events, common in the studied area, may favor the coexistence of species with different phenological strategies (Valim et al. 2013).Thus, care must be taken when generalizing the terminology "seasonal semideciduous forests" (Scolforo et al. 2008) for the forest of this park and similar surrounding areas.
The greatest species richness occurs in campos rupestres (almost 70%), with 61% of species occurring exclusively in this phytophysiognomy.The campo rupestre is a very old mountaintop ecosystem, being a museum of ancient lineages as well as a cradle of continuing diversification of endemic lineages (Silveira et al. 2016).The astonishing species richness found in the campos rupestres is favoured by the high environmental exploration, some farms in this area focused on agriculture, especially tea (Cammelia sinensis), Eucalyptus plantation for charcoal production and cattle.The tea was introduced in this area in the eighteenth and nineteenth centuries, playing a key role in the local economy.This activity lasted until the 50s, when the plantations were then abandoned (Fujaco et al. 2010).Thus, individuals of this species are still found in the vicinity of the old farm "Fazenda São José do Manso", where there was the largest planted area.Other significant anthropogenic impact occurred in the second half of XX century, with the aluminum (bauxite) mining.In addition, more recently urban sprawl has become one of the main threats alongside the Park, compromising the integrity of the surrounding environment (Fujaco et al. 2010).
Most of the exotic phanerogamic species occur in these anthropogenic disturbed areas.The most aggressive ones are Eucalyptus grandis, Hedychium coronarium and Melinis minutiflora.They have shown fast grown and high dispersal ability, easily increasing their population and spreading to other surrounding areas.Other exotic species observed didn't seem to present much competitiveness like Cammelia sinensis (tea), some ornamental plants like Hydrangea macrophylla, Impatiens balsamina and Rhododendron indicum.Probably, because most of the cultivated species are not able to grow in these metaliferous and nutrient-poor soils (Fernandes et al. 2016;Schaefer et al. 2016).Little is still known about biological invasion on mountaintop complexes where the threat of invasive species is very substantial (Wilson et al. 2016).Thus, more research is necessary about this subject.
Although Araucaria brasiliensis was considered initially as a naturally occurring species in this region (Mello-Barreto 1942, Hueck 1953), the observation of aerial photographs showed that the older individuals of this species were aligned, suggesting they were grown in this area.Further studies are still needed to clarify if this species is native to the Itacolomi State Park area.
A total of 79 species are threatened with extinction, being 57 species listed on the red list of Minas Gerais State (COPAM 1997), 40 figure on the Brazilian Red List (MMA 2014) and two others from IUCN Red List (2015).Most of them are described as vulnerable or endangered.However, some species are listed as critically endangered (CR) like Stevia hilarii, Valeriana organensis, Ocotea felix and Habenaria itaculumia on The Brazilian Red List (Table 1).Even though Trichogonia eupatorioides (=Trichogonia martii) and Trembleya calycina are described as probably extinct in the red list of the state of Minas Gerais (COPAM 1997), there are recent collections of these species in the herbarium databases (CRIA 2016).Other surveys along the Espinhaço Range have shown the same pattern, with many threatened species (Giulietti & Pirani 1988, Pirani et al. 1994, Echternacht et al. 2011).The campos rupestres show a high concentration of endemic species, some of them occur in small population (Giulietti & Pirani 1988, Echternacht et al. 2011).Thus, they are very vulnerable to extinction.
Some species are endemic to the Itacolomi State Park: Habenaria itaculumia and Heterocondylus itacolumiensis, in the campos rupestres and Cybianthus itacolomyensis in the forest.Other species are known as endemic to Espinhaço Range, in campos rupestres, like: Chamaecrista dentata, C. hedysaroides, C. rotundata, Cryptanthus schwackeanus, Mimosa aurivillus var.aurivillus, Aspilia caudata and Richterago hatschbachii (Flora do Brasil 2016, CRIA 2016).The high flora diversity of this Park, harboring more than 12% of the Angiosperm species known for Minas Gerais State(BFG 2015), as well as the many endemic and endangered species, shows the value of this conservation unit as one of the most important in the state of Minas Gerais and Brazil.The knowledge of phanerogamic flora of ISP can help the Management Plan of this Unit of Conservation, contribute to future works related in this area and also improve the understanding of the Minas Gerais and Brazilian flora.

Figure 5 .
Figure 5. Growth habit of the recorded phanerogamic species of the Itacolomi State Park, Ouro Preto and Mariana, Minas Gerais, Brazil.

Figure 4 .
Figure 4. Venn diagram showing the number of shared and exclusive phanerogamic species in the different habitats at Itacolomi State Park, Ouro Preto and Mariana, Minas Gerais, Brazil.AA= Antropogenic disturbed areas, CR= Campos rupestres, F=Montane forests.