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

Flora Fanerogâmica e Vegetação do Parque Estadual do Itacolomi, Minas Gerais, Brasil

Abstract

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.

Keywords:
Brazilian flora; campos rupestres; Iron Quadrangle flora; montane forests; rock outcrop flora; Neotropics

Resumo

O Parque Estadual do Itacolomi (PEIT) localiza-se nos municípios de Ouro Preto e Mariana, no Quadrilátero Ferrífero de Minas Gerais e abriga mais de 7.000 ha de remanescentes de mata atlântica e campos rupestres. A região do QF possui alta biodiversidade vegetal e está sobre alto impacto, principalmente pela mineração. O objetivo deste estudo foi apresentar a lista das espécies fanerogâmicas e os principais tipos vegetacionais desse Parque, no intuito de organizar a diversidade florística existente, além de servir como suporte para pesquisas correlatas subsequentes. O levantamento florístico foi realizado de outubro/1992 a julho/2006 por excursões mensais ao campo. Foram também incluídas na listagem registros ocorrentes em banco de dados de herbários. Foram identificados 1623 táxons, pertencentes à 122 famílias. As famílias mais representativas foram Asteraceae, Fabaceae, Melastomataceae, Poaceae e Orchidaceae. A vegetação do PEIT é constituída por campos rupestres (51% da área do parque), seguido pelas florestas montanas (40%) e por formações antrópicas (9%). A maior riqueza de espécies ocorre nos campos rupestres. Diversas espécies figuram em listas de espécies ameaçadas de extinção e outras são endêmicas. O conhecimento da flora fanerogâmica do Parque Estadual do Itacolomi pode subsidiar o Plano de Manejo dessa Unidade de Conservação e contribuir para futuros trabalhos correlatos nesta área, além de suprir conhecimentos para a flora de Minas Gerais e do Brasil.

Palavras-chave:
campos rupestres; flora do Quadrilátero Ferrífero; flora do Brasil; florestas montanas; Neotropicos

Introduction

Minas Gerais is the Brazilian State with the highest richness and endemism of Angiosperm species and harbors important phytogeographical domains (BFG 2015BFG 2015. Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085-1113.). Among them, the Atlantic Forest and the Cerrado are the largest, richest and more threatened ones (Fundação SOS Mata Atlântica 1998FUNDAÇÃO SOS MATA ATLÂNTICA. 1998. Atlas da evolução dos remanescentes florestais e ecossistemas associados no domínio da Mata Atlântica no Período 1990-1995. Fundação SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais / Instituto Socioambiental, São Paulo, Brasil., Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20:1-11.). 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 1998FUNDAÇÃO SOS MATA ATLÂNTICA. 1998. Atlas da evolução dos remanescentes florestais e ecossistemas associados no domínio da Mata Atlântica no Período 1990-1995. Fundação SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais / Instituto Socioambiental, São Paulo, Brasil.). In spite of the Atlantic Forest being considered a biodiversity hotspot (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., FONSECA, G.A.B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853-858.), it was reduced to less than 12% of its original size, with most of the remaining areas restricted to Conservation Units (Ribeiro et al. 2009RIBEIRO, M.C., METZGER, J.P., MARTENSEN, A.C., PONZONI, F. & HIROTA, M.M. 2009. Brazilian Atlantic forest: how much is left and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142:1141-1153.).

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 1988GIULIETTI, A.M. & PIRANI, J.R. 1988. Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In Workshop on Neotropical Distribution Patterns (W.R. Heyer & P.E Vanzolini, eds.). Academia Brasileira de Ciências, Rio de Janeiro, p.39-69.). Phytogeographically, the campos rupestres are classified into the Cerrado domain (Coutinho 2006COUTINHO, L.M. 2006. O conceito de bioma. Acta Bot. Bras. 20:1-11., Batalha 2011BATALHA, M.A. 2011. O cerrado não é um bioma. Biota Neotrop. 11:21-24.), 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. 2011ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C.T. & PIRANI, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782-791., 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. 1998COSTA, C.M.R., HERMANN, G., MARTINS, C.S., LINS, L.V. & LAMAS, I.R. 1998. Biodiversidade em Minas Gerais: um atlas para sua conservação. Fundação Biodiversitas, Belo Horizonte.). 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 km2, in the central portion of the Minas Gerais State (Dorr 1969DORR, J.V.N. 1969. Physiographic, stratigraphic and structural development of the Quadrilátero Ferrífero. Professional Paper, US Geological Survey 641-A, Washington.). This region is considered to be of extreme biological importance (Costa et al. 1998COSTA, C.M.R., HERMANN, G., MARTINS, C.S., LINS, L.V. & LAMAS, I.R. 1998. Biodiversidade em Minas Gerais: um atlas para sua conservação. Fundação Biodiversitas, Belo Horizonte.). 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. 2011ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C.T. & PIRANI, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782-791.). The Atlantic Forest in the QF Region is mainly represented by a seasonal semideciduous type (Morellato & Haddad 2000MORELLATO, L.P.C. & HADDAD, C.F.B. 2000. Introduction: The Brazilian Atlantic Forest. Biotropica 32:786-792.) 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. 2011MESSIAS, M.C.T.B., GARCIA, M.G.P., MEIRA NETO, J.A.A. & KOZOVITS, A.R. 2011. Life-form spectra of quartzite and itabirite rocky outcrop sites, Minas Gerais, Brazil. Biota Neotrop. 11:1-14., 2012MESSIAS, M.C.T.B., LEITE, M.G.P., MEIRA-NETO, J.A.A. & KOZOVITS, A.R. 2012. Fitossociologia de campos rupestres quartzíticos e ferruginosos no Quadrilátero Ferrífero, Minas Gerais. Acta Bot. Bras. 26:230-242., 2013MESSIAS, M.C.T.B., LEITE, M.G.P., MEIRA-NETO, J.A.A., KOZOVITS, A.R. & TAVARES, R. 2013. Soil-Vegetation Relationship in Quartzitic and Ferruginous Brazilian Rocky Outcrops Folia Geobot. 48:509-521.). Cangas are one of the most diverse, threatened and least studied ecosystems of southeast Brazil (Jacobi et al. 2007JACOBI, C.M., CARMO, F.F., VINCENT, R.C. & STEHMANN, J.R. 2007. Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers. Conserv. 16:2185-2200.). 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. 2007JACOBI, C.M., CARMO, F.F., VINCENT, R.C. & STEHMANN, J.R. 2007. Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers. Conserv. 16:2185-2200.).

Itacolomi State Park is one of the few full protection conservation units in this region (IEF 2016IEF. 2016. Parque Estadual do Itacolomi. http://www.ief.mg.gov.br/parques/itacolomi/itacolomi.asp (last access in Feb 15th, 2016)
http://www.ief.mg.gov.br/parques/itacolo...
) 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 1989PERON, M.V. 1989. Listagem preliminar da flora fanerogâmica dos Campos Rupestres do Parque Estadual do Itacolomi, Ouro Preto/Mariana, MG. Rodriguésia 67:63-69.), specific family studies about Orchidaceae (Alves 1990ALVES, R.J.V. 1990. The Orchidaceae of Itacolomi State Park in Minas Gerais, Brazil. Acta Bot. Bras. 4:65-72., Batista et al. 2004BATISTA, J.A.N., BIANCHETTI, L.B., NOGUEIRA, R.E., PELLIZZARO, K.F. & FERREIRA, F.E. 2004. The genus Habenaria (Orchidaceae) in the Itacolomi State Park, Minas Gerais, Brazil. Sitientibus, Série Ciências Biológicas 4:25-36.), Leguminosae (Dutra et al. 2005DUTRA, V.F., MESSIAS, M.C.T.B. & GARCIA, F.C.P. 2005. Papilionoideae (Leguminosae) dos campos ferruginosos do Parque Estadual do Itacolomi, MG, Brasil: florística e fenologia. Rev. Bras. Bot. 28:493-504., 2008aDUTRA, V.F., GARCIA, F.C.P. & LIMA, H.C. 2008a Mimosoideae (Leguminosae) nos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguésia 59:573-585., 2008bDUTRA, V.F., GARCIA, F.C.P. & LIMA, H.C. 2008b. Caesalpinioideae (Leguminosae) nos Campos Rupestres do Parque Estadual do Itacolomi, Estado de Minas Gerais, Brasil. Acta Bot. Brasilica 22:543-554., 2009DUTRA, V.F., GARCIA, F.C.P. & LIMA, H. 2009. Papilionoideae (Leguminosae) nos Campos Rupestres do Parque Estadual do Itacolomi, MG, Brasil. Acta Bot. Brasil. 23:145-159., 2014DUTRA, V.F.; LIMA, L.C.P.; GARCIA, F.C.P.; LIMA, H.C. & SARTORI, A.L.B. 2014. Geographic distribution patterns of Leguminosae and their relevance for the conservation of the Itacolomi State Park, Minas Gerais, Brazil. Biota Neotrop 14(1): e20133937., Lima et al. 2007LIMA, L.C.P., GARCIA, F.C.P. & SARTORI, A.L.B. 2007. Leguminosae nas florestas estacionais do Parque Estadual do Itacolomi, Minas Gerais, Brasil: ervas, arbustos, subarbustos, lianas e trepadeiras. Rodriguésia 58:331-358., 2010LIMA, L.C.P., GARCIA, F.C.P. & SARTORI, A.L.B. 2010. As Leguminosae arbóreas das florestas estacionais do Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguésia 61:441–466.), Bromeliaceae (Coser et al. 2010COSER, T.S., PAULA, C.C. & WENDT, T. 2010. Bromeliaceae Juss. nos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguésia 61:261-280.), Myrtaceae (Bünger et al. 2012BÜNGER, M.O., SCALON, V.R., SOBRAL, M. & STEHMANN, J.R. 2012. Myrtaceae no Parque Estadual do Itacolomi, Minas Gerais, Brasil. Rodriguésia 63:857-881.) and Asteraceae (Barnadesieae e Mutiseae) (Almeida et al. 2014ALMEIDA, G.S.S., CARVALHO-OKANO, R.M., NAKAJIMA, J.N. & GARCIA, F.C.P. 2014. Asteraceae Dumort nos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil: Barnadesieae e Mutisieae. Rodriguésia 65:311-328.). And also, few floristic studies have been recently published on small patches of campos rupestres (Gastauer et al. 2012GASTAUER, M., MESSIAS, M.C.T.B. & MEIRA-NETO, J.A.A. 2012. Floristic Composition, Species Richness and Diversity of Campo Rupestre Vegetation from the Itacolomi State Park, Minas Gerais, Brazil. Environment and Natural Resources Research 2:115-128.) and forests (Pedreira & Sousa 2011PEDREIRA, G. & SOUSA, H.C. 2011. Comunidade arbórea de uma mancha florestal permanentemente alagada e de sua vegetação adjacente em Ouro Preto-MG, Brasil. Cienc. Florest. 21:663-675.) 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.

Material and Methods

This survey was carried out in Itacolomi State Park (ISP), situated in the municipalities of Ouro Preto (World Patrimony by Unesco) and Mariana (Brazilian Historic Patrimony), Minas Gerais State, (43o32’30” to 43o22’30”W and 20o22’30” to 20o30’00”S). This Brazilian Conservation Unit was created in 1967 by Minas Gerais State law nº 4465 (Figure 1).

Figure 1
Vegetation map and location of the Itacolomi State Park (ISP), Ouro Preto and Mariana, Minas Gerais, Brazil. F = Montane Forest, CR = Campos rupestres, AA = Anthropogenic disturbed areas.

According to Peron (1989)PERON, M.V. 1989. Listagem preliminar da flora fanerogâmica dos Campos Rupestres do Parque Estadual do Itacolomi, Ouro Preto/Mariana, MG. Rodriguésia 67:63-69. 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. 2013ÁLVARES, C.A., STAPE, J.L., SENTELHAS, P.C., GONÇALVES, J.L.M. & SPAROVEK, G. 2013. Köppen's climate classification map for Brazil. Meteorol Z. 22:711-728.). 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 1993CASTAÑEDA, C. 1993. Caracterização geológica e geomorfológica do Parque Estadual de Itacolomi. Projeto Itacolomi, Convênio IEF/UFOP/BIRD. Technical Report. Universidade Federal de Ouro Preto, Ouro Preto.). 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 1993CASTAÑEDA, C. 1993. Caracterização geológica e geomorfológica do Parque Estadual de Itacolomi. Projeto Itacolomi, Convênio IEF/UFOP/BIRD. Technical Report. Universidade Federal de Ouro Preto, Ouro Preto.). 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 2016CRIA Centro de Referência em Informação Ambiental. 2016. speciesLink. http://splink.cria.org.br/ (last access in July 1th, 2016).
http://splink.cria.org.br/...
) and JABOT (JBRJ 2016JBRJ - Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. 2016. Jabot - Banco de Dados da Flora Brasileira. http://www.jbrj.gov.br/jabot (last access in Jun 15th, 2016).
http://www.jbrj.gov.br/jabot...
) 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)THIERS, B. 2016. [continuously updated]. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. http://sweetgum.nybg.org/science/ih/ (last access in Oct 10st, 2016).
http://sweetgum.nybg.org/science/ih/...
.

The circumscription of families followed the Angiosperm Phylogeny Group - APG III (Chase & Reveal 2009CHASE, M.W. & REVEAL, J.L. 2009. A phylogenetic classification of the land plants to accompany APG III. Bot. J. Lin. Soc. 161:122-127.). The species names were checked with the database of the list of species of the Brazilian Flora 2020 Project (2016)FLORA DO BRASIL 2020 em construção. 2016. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/reflora/listaBrasil/ConsultaPublicaUC/ConsultaPublicaUC.do#CondicaoTaxonCP (last access in May 24th, 2016).
http://floradobrasil.jbrj.gov.br/reflora...
and The Plant List (2013)THE PLANT LIST. 2013. Version 1.1. http://www.theplantlist.org (last access in Jan 21st, 2016).
http://www.theplantlist.org...
. Each species was described by its habit (Rizzini 1997RIZZINI, C.T. 1997. Tratado de fitogeografia do Brasil: aspectos ecológicos, sociológicos e florísticos. Âmbito Cultural, Rio de Janeiro.) and habitat. The forest vegetation was classified according to Veloso et al. (1991)VELOSO, H.P., RANGEL-FILHO, A.L.R. & LIMA, J.C.A. 1991. A classificação da vegetação brasileira adaptada a um sistema universal. IBGE, Rio de Janeiro. and the grasslands areas followed Ferri (1980)FERRI, M.G. 1980. Vegetação brasileira. EDUSP, São Paulo., Eiten (1983)EITEN, G. 1983. Classificação da vegetação do Brasil. Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasília. and Giulietti et al. (1987)GIULIETTI, A.M., MENEZES, N.M., PIRANI, J.R., MEGURO, M. & WANDERLEY, M.G.L. 1987. Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Bol. Bot. Univ. São Paulo 9:1-51.. 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 2014MINISTÉRIO DO MEIO AMBIENTE (MMA). 2014. Portaria No 443, de 17 de dezembro de 2014. Lista nacional oficial de espécies da flora ameaçadas de extinção. http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=18/12/2014&jornal=1&pagina=110&totalArquivos=144 (last access in Feb 15th, 2015).
http://pesquisa.in.gov.br/imprensa/jsp/v...
) and Minas Gerais (COPAM 1997COPAM. 1997. Deliberação COPAM nº 85, 30 de outubro de 1997. Conselho Estadual de Política Ambiental, Belo Horizonte.) 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, 2007ENVIRONMENTAL SYSTEMS RESEARCH INSTITUTE. 2007. ArcEditor - Desktop GIS with advanced geographic data editing and management. http://www.esri.com/software/arcgis/arceditor/index.html (last access in Jan 24th, 2007).
http://www.esri.com/software/arcgis/arce...
).

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. 1995STANNARD, B.L. 1995. Flora of the Pico das Almas, Chapada Diamantina, Bahia, Brazil. Kew, Royal Botanic Gardens.), Ibitipoca: 1080 species (Forzza et al. 2013FORZZA, R.C., MENINI-NETO L., SALIMENA, F.R.G. & ZAPPI, D. 2013. Fanerógamas do Parque Estadual do Ibitipoca e suas relações florísticas com outras áreas com campo rupestre de Minas Gerais. In Flora do Parque Estadual de Ibitipoca e seu entorno (R.C. Forzza, L. Menini-Neto, F.R.G. Salimena & D. Zappi, Orgs.) Editora UFJF, Juiz de Fora, p.153-292.), Grão Mogol: 1073 species (Pirani et al. 2003PIRANI, J.R., MELLO-SILVA, R. & GIULIETTI, A.M. 2003. Flora de Grão-Mogol, Minas Gerais, Brasil. Bol. Bot. Univ. São Paulo 21:1-24.), Serra de São José: 1087 species (Alves & Kolbek 2009ALVES, R.J.V. & KOLBEK, J. 2009. Summit vascular flora of Serra de São José, Minas Gerais, Brazil. Check List 5:35-73.) and Serra do Cipó: 1530 species (Giulietti et al. 1987GIULIETTI, A.M., MENEZES, N.M., PIRANI, J.R., MEGURO, M. & WANDERLEY, M.G.L. 1987. Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Bol. Bot. Univ. São Paulo 9:1-51.). These results highlight how diverse is the ISP flora as well as the importance of focusing on further taxonomic studies in this park.

Table 1
Checklist of phanerogamic species of Itacolomi State Park, Ouro Preto/Mariana, Minas Gerais, Brazil and their respective habit, habitat and voucher (Herbarium acronym + number). Habitat: F = Montane forest, CR = Campos rupestres, AA = Anthropogenic disturbed areas. After the species name, in red, the categories of threatened species and references: CR = Critically endangered, DD = Data deficient, EN = Endangered, EX = Probably Extinct, LC = Least concern, NT = Near threatened, VU = Vulnerable, * COPAM (1997)COPAM. 1997. Deliberação COPAM nº 85, 30 de outubro de 1997. Conselho Estadual de Política Ambiental, Belo Horizonte., ** MMA (2014)MINISTÉRIO DO MEIO AMBIENTE (MMA). 2014. Portaria No 443, de 17 de dezembro de 2014. Lista nacional oficial de espécies da flora ameaçadas de extinção. http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=18/12/2014&jornal=1&pagina=110&totalArquivos=144 (last access in Feb 15th, 2015).
http://pesquisa.in.gov.br/imprensa/jsp/v...
, *** IUCN (2015)IUCN 2015. The IUCN Red List of Threatened Species. Version 2015-4. http://www.iucnredlist.org (last access in Nov 12th, 2015).
http://www.iucnredlist.org...
.

The families with higher species richness were Asteraceae (323), Fabaceae (154), Melastomataceae (131), Poaceae (84), Orchidaceae (62), Myrtaceae (58) and Bignoniaceae (57), represent more than 75% of the total sampled species (Figure 2). The richness of these families was also reported in other campos rupestres (Harley & Simmons 1986HARLEY, R.M. & SIMMONS, N.A. 1986. Florula of Mucugê, Chapada Diamantina – Bahia, Brazil. Royal Botanic Gardens, Kew., Giulietti et al. 1987GIULIETTI, A.M., MENEZES, N.M., PIRANI, J.R., MEGURO, M. & WANDERLEY, M.G.L. 1987. Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Bol. Bot. Univ. São Paulo 9:1-51., 1997, Pirani et al. 1994PIRANI, J.R., GIULIETTI, A.M., MELLO-SILVA, R. & MEGURO, M. 1994. Checklist and patterns of geographic distribution of the vegetation of Serra do Ambrósio, Minas Gerais, Brazil. Rev. Bras. Bot.17:133-147., Conceição & Giulietti 2002CONCEIÇÃO, A.A. & GIULIETTI, A.M. 2002. Composição florística e aspectos estruturais de campo rupestre em dois platôs do Morro do Pai Inácio, Chapada Diamantina, Bahia, Brasil. Hoehnea 29:37-48., Conceição & Pirani 2005CONCEIÇÃO, A.A. & PIRANI, J.R. 2005. Delimitação de habitats em campos rupestres na Chapada Diamantina, Bahia: Substratos, composição florística e aspectos estruturais. Bol. Bot. Univ. São Paulo 23:85-111., Jacobi & Carmo 2012CARMO, F.F. & JACOBI, C.M. 2012 The cangas of the Iron Quadrangle. In Floristic diversity of the Quadrilátero Ferrífero cangas (C.M. Jacobi & F.F. Carmo, Eds.) IDM, Belo Horizonte, p.14-30., Messias et al. 2012MESSIAS, M.C.T.B., LEITE, M.G.P., MEIRA-NETO, J.A.A. & KOZOVITS, A.R. 2012. Fitossociologia de campos rupestres quartzíticos e ferruginosos no Quadrilátero Ferrífero, Minas Gerais. Acta Bot. Bras. 26:230-242., Forzza et al. 2013FORZZA, R.C., MENINI-NETO L., SALIMENA, F.R.G. & ZAPPI, D. 2013. Fanerógamas do Parque Estadual do Ibitipoca e suas relações florísticas com outras áreas com campo rupestre de Minas Gerais. In Flora do Parque Estadual de Ibitipoca e seu entorno (R.C. Forzza, L. Menini-Neto, F.R.G. Salimena & D. Zappi, Orgs.) Editora UFJF, Juiz de Fora, p.153-292.). Fabaceae, Myrtaceae, Melastomataceae and Asteraceae are also species-rich families in Espinhaço Range forests (Kamino et al. 2008KAMINO, L.H.Y., OLIVEIRA-FILHO, A.T. & STEHMANN, J.R. 2008. Relações florísticas entre as fitofisionomias florestais da Cadeia do Espinhaço, Brasil. Megadiversidade 4:38-77.). However, comparing with the data presented by these authors, Bignoniaceae and Solanaceae presented higher tree species richness in ISP than in other Espinhaço Range forests. Almeida et al. (2014)ALMEIDA, G.S.S., CARVALHO-OKANO, R.M., NAKAJIMA, J.N. & GARCIA, F.C.P. 2014. Asteraceae Dumort nos campos rupestres do Parque Estadual do Itacolomi, Minas Gerais, Brasil: Barnadesieae e Mutisieae. Rodriguésia 65:311-328. studying Asteraceae of ISP, described three new species and considered this Park as the richest Brazilian one for Asteraceae. Many families (29) are represented by only one species, what has been reported in other surveys along the Espinhaço Range (Giulietti et al. 1987GIULIETTI, A.M., MENEZES, N.M., PIRANI, J.R., MEGURO, M. & WANDERLEY, M.G.L. 1987. Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Bol. Bot. Univ. São Paulo 9:1-51., 1997, Pirani et al.1994PIRANI, J.R., GIULIETTI, A.M., MELLO-SILVA, R. & MEGURO, M. 1994. Checklist and patterns of geographic distribution of the vegetation of Serra do Ambrósio, Minas Gerais, Brazil. Rev. Bras. Bot.17:133-147., 2003PIRANI, J.R., MELLO-SILVA, R. & GIULIETTI, A.M. 2003. Flora de Grão-Mogol, Minas Gerais, Brasil. Bol. Bot. Univ. São Paulo 21:1-24.).

Figure 2
Fanerogamic species-richest families in the Itacolomi State Park, Ouro Preto and Mariana, Minas Gerais, Brazil.

The campos rupestres represent 51% of the total area, followed by the forest with 40% and anthropogenic disturbed areas with 9% (Figure 1). The vegetation seems to be closely associated with geology, geomorphology, depth and moisture of the soil, as well as the degree of anthropogenic impact, resulting in a variety of different physiognomies (Figure 3), similarly to other montane areas (Benites et al. 2007BENITES, V.M., SCHAEFER, C.E.G.R., SIMAS, F.N.B. & SANTOS, H.G. 2007. Soils associated with rock outcrops in the Brazilian mountain ranges Mantiqueira and Espinhaço. Rev. Bras. Bot. 30:569-577.; Schaefer et al. 2016SCHAEFER, C.E.G.R., CORRÊA, G.R., CANDIDO, H.G., ARRUDA, D.M., NUNES, J.A., ARAUJO, R.W., RODRIGUES, P.M.S., FERNANDES FILHO, E.I., PEREIRA, A.F.S. BRANDÃO, P.C. & NERI, A.V. The Physical Environment of Rupestrian Grasslands (Campos Rupestres) in Brazil: Geological, Geomorphological and Pedological Characteristics, and Interplays. In Ecology and Conservation of Mountaintop Grasslands in Brazil (G.W. Wilson, Ed.). Springer, Switzerland, p.15-40.). The campos 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.

Figure 3
Phytophysiognomies of Itacolomi State Park, Ouro Preto and Mariana, Minas Gerais, Brazil. A. Itacolomi Peak surrounded by campos rupestres; B. Partial view of the Itacolomi State Park (ISP), with campos rupestres and forest patches; C. Monodominant forest made up of “Candeia” (Eremanthus erythropappus); D. Partial view of a ferruginous campo rupestre; E-F. Quartzitic campos rupestres.

The forests at Itacolomi State Park have the same pattern of the forests along the Espinhaço Range (Harley 1995HARLEY, R.M. 1995. Introduction. In Flora of the Pico das Almas, Chapada Diamantina - Bahia, Brazil. (B.L. Stannard, Y.B. Harvey & R.M. Harley, eds.). Royal Botanic Gardens, Kew, p.1-42.), 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)KAMINO, L.H.Y., OLIVEIRA-FILHO, A.T. & STEHMANN, J.R. 2008. Relações florísticas entre as fitofisionomias florestais da Cadeia do Espinhaço, Brasil. Megadiversidade 4:38-77., a riparian forest on the valleys may be evergreen, while the adjacent forest on the slope is semideciduous. In fact, Pedreira & Sousa (2011)PEDREIRA, G. & SOUSA, H.C. 2011. Comunidade arbórea de uma mancha florestal permanentemente alagada e de sua vegetação adjacente em Ouro Preto-MG, Brasil. Cienc. Florest. 21:663-675. 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 1984REICH, P.B. & BORCHET, R. 1984. Water stress and tree phenology in a tropical dry forest in the lowlands of Costa Rica. J. Ecol. 72:61-74., Lenza & Klink 2006LENZA, E. & KLINK, C.A. 2006. Comportamento fenológico de espécies lenhosas em um cerrado sentido restrito de Brasília, DF. Rev. Bras. Bot. 29:627-638.). However, the fog events, common in the studied area, may favor the coexistence of species with different phenological strategies (Valim et al. 2013VALIM, E.A.R., NALINI-JR, H.A. & KOZOVITS, A.R. 2013. Litterfall dynamics in a iron-rich rock outcrop complex in the southeastern portion of the Iron Quadrangle of Brazil. Acta Bot. Brasilica 27:286-293.). Thus, care must be taken when generalizing the terminology “seasonal semideciduous forests” (Scolforo et al. 2008SCOLFORO, J.R.S., MACHADO, E.L.M., SILVA, C.P.C., MELLO, J.M. & OLIVEIRA-FILHO, A.T. 2008. Definição de grupos fisionômicos na floresta estacional semidecidual e na floresta ombrófila. In Inventário Florestal de Minas Gerais: Floresta estacional semidecidual e ombrófila - Florística, estrutura, diversidade, similaridade, distribuição diamétrica e de altura, volumetria, tendências de crescimento e áreas aptas para manejo florestal (J.R.S. Scolforo, J.M. Mello & C.P.C. Silva, eds.). Editora UFLA, Lavras, cap. 1, p.91-192.) 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 diversity, wide latitudinal and altitudinal range, isolation and influence of different vegetation domains (Giulietti et al. 1997GIULLIETI, A.M., PIRANI, J.R. & HARLEY, R.M. 1997. Espinhaço Range region, Eastern Brazil. In Centres of plant diversity: a guide and strategy for their conservation. (S.D. Davis, V.H. Heywood, O. Herrera-Macbride, J. Villa-Lobos & A.C. Hamilton, eds). Information Press, Oxford, p.397-404., Jacobi et al. 2007JACOBI, C.M., CARMO, F.F., VINCENT, R.C. & STEHMANN, J.R. 2007. Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers. Conserv. 16:2185-2200., Silveira et al. 2016).

The forests house about 36% of the species and 7% of the species occur in both physiognomies (forest and campos rupestres) like Eremanthus erythropappus, Schinus terebinthifolius, Clethra scabra, Vochysia tucanorum, among others. Some species occur just in anthropogenic disturbed areas (1.8%) (Table 1, Figure 4). Some species found in the forests like Hedyosmum brasiliense, Laplacea fructicosa, Drimys brasiliensis, Weinmamania pauliniiflora and Ocotea percoriacea are typical of Brazilian montane forests (CRIA 2016CRIA Centro de Referência em Informação Ambiental. 2016. speciesLink. http://splink.cria.org.br/ (last access in July 1th, 2016).
http://splink.cria.org.br/...
).

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.

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. 2011ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C.T. & PIRANI, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782-791.). 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, 2011FERREIRA M.T.M. 2011. Composição florística e distribuição vertical de epífitas vasculares sobre indivíduos de Guapira opposita (Vell) Reitz (Nyctaginaceae) em um fragmento florestal na Serra da Brígida, Ouro Preto, MG. Master Dissertation, Federal University of Ouro Preto.).

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

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 1999OLIVEIRA-FILHO, A.T. & FLUMINHAN-FILHO, M. 1999. Ecologia da vegetação do Parque Florestal Quedas do Rio Bonito. Cerne 5:50-63., Kamino et al. 2008KAMINO, L.H.Y., OLIVEIRA-FILHO, A.T. & STEHMANN, J.R. 2008. Relações florísticas entre as fitofisionomias florestais da Cadeia do Espinhaço, Brasil. Megadiversidade 4:38-77.). 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 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. 2010FUJACO, M.A.G., LEITE, M.G.P. & MESSIAS, M.C.T.B. 2010. Análise multitemporal das mudanças no uso e ocupação do Parque Estadual do Itacolomi (MG) através de técnicas de geoprocessamento. R. Esc. Min. 63: 695-701.). 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. 2010FUJACO, M.A.G., LEITE, M.G.P. & MESSIAS, M.C.T.B. 2010. Análise multitemporal das mudanças no uso e ocupação do Parque Estadual do Itacolomi (MG) através de técnicas de geoprocessamento. R. Esc. Min. 63: 695-701.).

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. 2016FERNANDES, G.W., TOMA, T.S.P, ANGRISANO, P. & OVERBECK, G. Challenges in the Restoration of Quartzitic and Ironstone Rupestrian Grasslands. In Ecology and conservation of mountaintop grasslands in Brazil (G.W. Fernandes, Ed.) Springer, Switzerland, p.449-478.; Schaefer et al. 2016SCHAEFER, C.E.G.R., CORRÊA, G.R., CANDIDO, H.G., ARRUDA, D.M., NUNES, J.A., ARAUJO, R.W., RODRIGUES, P.M.S., FERNANDES FILHO, E.I., PEREIRA, A.F.S. BRANDÃO, P.C. & NERI, A.V. The Physical Environment of Rupestrian Grasslands (Campos Rupestres) in Brazil: Geological, Geomorphological and Pedological Characteristics, and Interplays. In Ecology and Conservation of Mountaintop Grasslands in Brazil (G.W. Wilson, Ed.). Springer, Switzerland, p.15-40.). 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 1942MELLO-BARRETO, H.L. 1942. Regiões fitogeográficas de Minas Gerais. Boletim do Departamento Geográfico de Minas Gerais 4:9-30., Hueck 1953HUECK, K. 1953. Distribuição e habitat natural do Pinheiro do Paraná (Araucaria angustifolia). Bol. Fac. Filos. Ciênc. Univ. São Paulo, Bot. 10:1-24.), 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 1997COPAM. 1997. Deliberação COPAM nº 85, 30 de outubro de 1997. Conselho Estadual de Política Ambiental, Belo Horizonte.), 40 figure on the Brazilian Red List (MMA 2014MINISTÉRIO DO MEIO AMBIENTE (MMA). 2014. Portaria No 443, de 17 de dezembro de 2014. Lista nacional oficial de espécies da flora ameaçadas de extinção. http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?data=18/12/2014&jornal=1&pagina=110&totalArquivos=144 (last access in Feb 15th, 2015).
http://pesquisa.in.gov.br/imprensa/jsp/v...
) 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 1997COPAM. 1997. Deliberação COPAM nº 85, 30 de outubro de 1997. Conselho Estadual de Política Ambiental, Belo Horizonte.), there are recent collections of these species in the herbarium databases (CRIA 2016CRIA Centro de Referência em Informação Ambiental. 2016. speciesLink. http://splink.cria.org.br/ (last access in July 1th, 2016).
http://splink.cria.org.br/...
). Other surveys along the Espinhaço Range have shown the same pattern, with many threatened species (Giulietti & Pirani 1988GIULIETTI, A.M. & PIRANI, J.R. 1988. Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In Workshop on Neotropical Distribution Patterns (W.R. Heyer & P.E Vanzolini, eds.). Academia Brasileira de Ciências, Rio de Janeiro, p.39-69., Pirani et al. 1994PIRANI, J.R., GIULIETTI, A.M., MELLO-SILVA, R. & MEGURO, M. 1994. Checklist and patterns of geographic distribution of the vegetation of Serra do Ambrósio, Minas Gerais, Brazil. Rev. Bras. Bot.17:133-147., Echternacht et al. 2011ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C.T. & PIRANI, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782-791.). The campos rupestres show a high concentration of endemic species, some of them occur in small population (Giulietti & Pirani 1988GIULIETTI, A.M. & PIRANI, J.R. 1988. Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In Workshop on Neotropical Distribution Patterns (W.R. Heyer & P.E Vanzolini, eds.). Academia Brasileira de Ciências, Rio de Janeiro, p.39-69., Echternacht et al. 2011ECHTERNACHT, L., TROVÓ, M., OLIVEIRA, C.T. & PIRANI, J.R. 2011. Areas of endemism in the Espinhaço Range in Minas Gerais, Brazil. Flora 206:782-791.). 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 2016FLORA DO BRASIL 2020 em construção. 2016. Jardim Botânico do Rio de Janeiro. http://floradobrasil.jbrj.gov.br/reflora/listaBrasil/ConsultaPublicaUC/ConsultaPublicaUC.do#CondicaoTaxonCP (last access in May 24th, 2016).
http://floradobrasil.jbrj.gov.br/reflora...
, CRIA 2016CRIA Centro de Referência em Informação Ambiental. 2016. speciesLink. http://splink.cria.org.br/ (last access in July 1th, 2016).
http://splink.cria.org.br/...
).

The high flora diversity of this Park, harboring more than 12% of the Angiosperm species known for Minas Gerais State (BFG 2015BFG 2015. Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085-1113.), 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.

Acknowledgements

This paper is dedicated to the memory of Jorge Luiz da Silva. The authors wish to thank to FAPEMIG and IEF/PROFLORESTA by the financial support and also to the taxonomists A. Rapini (Apocynaceae), G.S.S. Almeida and J. Nakajima (Asteraceae), V.F. Dutra (Fabaceae), D. Medeiros (Euphorbiaceae), P.L. Moraes (Lauraceae), M. Sobral and M.O.Bünger (Myrtaceae), M.A.M. Azevedo (Passifloraceae), M.F. Freitas (Primulaceae), R. Marquete (Salicaceae), J.R. Stehmann (Solanaceae), J.L. Aranha-Filho (Symplocaceae). Acknowledgements are also given to Alberto V. M. Matos (IEF) for his assistance during field work.

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Publication Dates

  • Publication in this collection
    2017

History

  • Received
    27 July 2016
  • Reviewed
    04 Jan 2017
  • Accepted
    05 Jan 2017
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