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Inventory • Biota Neotrop. 21 (1) • 2021 • https://doi.org/10.1590/1676-0611-BN-2020-1024   copy

Vascular plant checklist in an area of extreme biological importance: filling gaps in the Caparaó National Park-ES, Brazil

Checklist de plantas vasculares em uma área de extrema importância biológica: preenchendo lacunas no Parque Nacional do Caparaó-ES, Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Regional floristic lists are essential for defining biodiversity conservation strategies and are key to assist in filling knowledge gaps. They aim to provide a data source for applying tools to reduce extinction rates and to conserve ecosystems. Herein we present the results of an inventory of vascular plants in a rainforest in the Caparaó National Park (CNP) and approach their implications for conservation and management of this protected area and the surrounding communities. We conducted botanical expeditions between the years 2012 and 2017 in a montane and upper-montane forest of the CNP. We found 361 species distributed in 78 families and 181 genera. The study area is home to new species for science that have recently been described in other publications outside that location, and 4 new records for Espírito Santo State; also 43 species listed in different extinction threat categories (VU, EN and CR) and another 190 categorized with lesser concerns (LC and NT). The families with the highest species richness were: Melastomataceae (41 spp.), Lauraceae and Myrtaceae (30), Orchidaceae (26), Rubiaceae (24), and Asteraceae (20). Our results contribute to greater knowledge of the CNP flora, of the montane environments in Brazil and the vegetation of Espírito Santo state, in addition to demonstrate the importance of this protected area to the conservation Atlantic Forest biodiversity.

Keywords:
Neotropical region; Atlantic Forest; nature conservation; endangered species; regional flora

Resumo

As listas florísticas regionais são essenciais para definir estratégias de conservação da biodiversidade e importantes instrumentos para preencher lacunas de conhecimento. O objetivo foi fornecer uma base de dados a partir de uma listagem de espécies como ferramenta para conservação e manejo do ecossistema. Apresentamos aqui os resultados de um inventário de plantas vasculares em uma Floresta Ombrófila Densa no Parque Nacional Caparaó e abordamos suas implicações para a conservação e manejo desta área protegida e das comunidades do entorno. Realizamos expedições botânicas entre os anos de 2012 e 2017 na vertente capixaba dessa floresta ombrófila no parque. Foram encontradas 361 espécies distribuídas em 78 famílias e 181 gêneros. A área de estudo abriga novas espécies para ciência que foram recentemente descritas em outras publicações fora dessa localidade, e 4 novos registros para o Espírito Santo; também 43 espécies listadas em diferentes categorias de ameaça de extinção (VU, EN, CR) e outras 190 categorizadas com menores preocupações (LC e NT). As famílias com maior riqueza de espécies foram: Melastomataceae (41 spp.), Lauraceae e Myrtaceae (30), Orchidaceae (26), Rubiaceae (24) e Asteraceae (20). Nossos resultados contribuem para um maior conhecimento da flora do Parque, dos ambientes montanos no Brasil e da vegetação do Espírito Santo, além de demonstrar a importância dessa área protegida para a conservação da biodiversidade da Mata Atlântica.

Palavras-chave:
Região neotropical; Floresta Atlântica; conservação da natureza; espécies ameaçadas

Introduction

Regional floristic listings consist of important tools for designing conservation plans and actions for different ecosystems, and forms the essential basis for biodiversity management, developing of regional flora projects, supporting knowledge expansion. Despite the need for cataloguing biological diversity globally, especially in biodiversity hotspots (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. doi: 10.1038/35002501
https://doi.org/10.1038/35002501... , Mittermeier et al. 2004MITTERMEIER, R.A., ROBLES GIL, P., HOFFMANN, M. & et al. (eds). 2004. Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. CEMEX, Cidade do México.), the number of large expeditions like those carried out in the past by great naturalists, for instance, von Martius, Saint Hilaire and more recently A.C. Brade, were considerably reduced (Christenhusz & Byng 2016CHRISTENHUSZ, M.J.M. & BYNG, J.W. 2016. The number of known plants species in the world and its annual increase. Phytotaxa 261 (3): 201. doi: 10.11646/phytotaxa.261.3.1
https://doi.org/10.11646/phytotaxa.261.3... ) and there are no more. However, regional floristic surveys have been growing in the tropical region, enabling estimation of plant species richness in these tropical regions (Slik et al. 2015SLIK, J.W.F., ARROYO-RODRÍGUEZ ,V., AIBA, S.I. & et al. 2015. An estimate of the number of tropical tree species. P Natl Acad Sci-Biol 112 (24): 7472-7477. doi: 10.1073/pnas.1423147112
https://doi.org/10.1073/pnas.1423147112... ).

Brazil is the country that has the greatest plant richness in the world, with an estimated 34,459 species of vascular plants (BFG 2018). However, the state of knowledge on flora is still incipient in many regions of the country, as occurs in the Atlantic Forest, including protected areas (Lima et al. 2015LIMA, R.A.F., MORI, D.P., PITTA, G., MELITO, M.O., MAGNAGO, L.F., ZWIENER, V.P., SARAIVA, D.D., MARQUES, M.C.M., OLIVEIRA, A.A. & PRADO, P.I. 2015. How much do we know about the endangered Atlantic Forest? Reviewing nearly 70 years of information on tree community surveys. Biodivers Conserv 24: 2135-2148. doi: 10.1007/s10531-015-0953-1
https://doi.org/10.1007/s10531-015-0953-... , Zappi et al. 2016ZAPPI, D.C., MILLIKEN, W., LOPES, C.R.A.S., LUCAS, E., PIVA, J.H., FRISBY, S., BIGGS, N. & FORZZA, R.C. 2016. Xingu State Park vascular plant survey: filling the gaps. Braz J Bot 39: 751-778. doi: 10.1007/s40415-016-0262-2
https://doi.org/10.1007/s40415-016-0262-... , Oliveira et al. 2017OLIVEIRA, U., SOARES-FILHO, B.S., PAGLIA, A.P. & et al. 2017. Biodiversity conservation gaps in the Brazilian protected areas. Sci Rep-UK 7: 9141. doi: 10.1038/s41598-017-08707-2
https://doi.org/10.1038/s41598-017-08707... ), which have the conservation of plant species among their goals. Despite this, many species of vascular plants are listed as “data deficient” (Sousa-Baena et al. 2014), compromising actions for their conservation.

The lack of floristic studies in forest remnants in Brazil, especially those in which the access is difficult higher, such as mountain areas, leads to a lack of data in estimating the richness, as well as the occurrence of species (Giulietti et al. 2009GIULIETTI, A.M., RAPINI, A., ANDRADE, M.J.G. DE, QUEIROZ, L.P. DE & SILVA, J.M.C. (eds). 2009. Plantas raras do Brasil. Conservação Internacional, Belo Horizonte, MG, Brasil. 496 p.). Thus, the restricted knowledge on the distribution of species due to the low number of floristic inventories in some regions creates gaps and makes it harder to make decisions of public politics, since these studies work as tools for identifying potential places for the conservation, or even for establishing new strategies in areas already under protection regimes (IUCN 2017). Floristic inventories, in addition to generating information about the species composition of a certain area, also enable the feed a database that will serve as the basis for other taxonomic and ecologic studies, as well as studies on the restoration of degraded areas (Souza et al. 2009SOUZA, M., KAWAKITA, K., SLUSARSKI, S. & PEREIRA, G. 2009. Vascular flora of the Upper Paraná River floodplain. Braz J Biol 69 (2): 735-745. doi: 10.1590/S1519-69842009000300027
https://doi.org/10.1590/S1519-6984200900... ).

Given these justifications and for being recognized as an important Atlantic Forest remnant, as well as being in a priority area for conservation and having extremely high biological importance (Ministério do Meio Ambiente - MMA 2007), the efforts to know the flora in the Caparaó National Park (CNP) has started with the pioneering study by Brade (1942BRADE, A.C. 1942. Excursão à Serra do Caparaó, Minas Gerais. Rodriguesia 6: 87-92.) has been expanding over the last decade (Mazine & Souza 2008MAZINE, F.F. & SOUZA, V.C. 2008. Myrtaceae dos campos de altitude do Parque Nacional do Caparaó - Espírito Santo/Minas Gerais, Brasil. Rodriguesia 59 (1): 57-74. doi: 10.1590/2175-7860200859102
https://doi.org/10.1590/2175-78602008591... ; Forster & Souza 2013FORSTER, W. & SOUZA, V.C. 2013. Laeliinae (Orchidaceae) do Parque Nacional do Caparaó, Estados do Espírito Santo e Minas Gerais, Brasil. Hoehnea 40 (4): 701-726. doi: 10.1590/S2236-89062013000400010
https://doi.org/10.1590/S2236-8906201300... , Couto et al. 2016COUTO, D.R., DIAS, H.M., PEREIRA, M.C.A., FRAGA, C.N. & PEZZOPANE, J.E.M. 2016. Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops (inselbergs) in Brazilian Atlantic Rainforest: basis for conservation of a threatened ecosystem. Rodriguesia 67(3): 583-601., Machado et al. 2016MACHADO, T.M., FORZZA, R.C. & STEHMANN, J.R. 2016. Bromeliaceae from Caparaó National Park, Minas Gerais/Espírito Santo states, Brazil, with notes on distribution and conservation. Oecol Aust 20 (2): 271-284. doi: 10.4257/oeco.2016.2002.10
https://doi.org/10.4257/oeco.2016.2002.1... , Zorzanelli et al 2016ZORZANELLI, J.P.F., DIAS, H.M., DA SILVA, N.R. & KUNZ, S.H. 2016. Richness, structure and vegetation relationships of the woody layer in an upper montane forest in Caparaó National Park, Minas Gerais State, Brazil. Oecol Aust 20 (2): 177-183. doi: 10.4257/oeco.2016.2002.13
https://doi.org/10.4257/oeco.2016.2002.1... , Araujo et al. 2018ARAÚJO, E.A., KUNZ, S.H., DIAS, H.M., CARRIJO, T.T. & ZORZANELLI, J.P.F. 2018. Inventários florísticos na região do Caparaó Capixaba revelam novos registros para a flora do Espírito Santo. Rodriguesia 69 (4): 1953-1963. doi: 10.1590/2175-7860201869429
https://doi.org/10.1590/2175-78602018694... , Campos et al. 2018CAMPOS, P.V., VILLA, P.M., NUNES, J.A., SCHAEFER, C.E.R.G., POREMBSKI, S. & NERI, A.V. 2018. Plant diversity and community structure of Brazilian Páramos. J. Mt. Sci. 15(6): 1186-1198. doi: 10.1007/s11629-017-4674-7
https://doi.org/10.1007/s11629-017-4674-... ), beyond fascicles published by the herbarium “Guido Pabst” (GFJP). Recently, the list of plants from CNP was made available on the digital platform “Catálogo de Plantas das Unidades de Conservação do Brasil” (https://catalogo-ucs-brasil.jbrj.gov.br/), where there are 1,789 species of 714 genera and 198 botanical families, of these, 1,292 are angiosperms, 37 lycophytes, 262 ferns and 198 are avascular plants (Carrijo et al. 2020CARRIJO, T.T., ALVES-ARAÚJO, A.G., AMORIM, A.M.A., ANTAR, G.M., et al. 2020. Lista de espécies de plantas terrestres do Parque Nacional do Caparaó. In: Catálogo de Plantas das Unidades de Conservação do Brasil. Jardim Botânico do Rio de Janeiro. Disponible: [https://catalogo-ucs-brasil.jbrj.gov.br]. last acess in 29/jul/2020.
https://catalogo-ucs-brasil.jbrj.gov.br... ).

Therefore, herein we present the results of a floristic inventory of vascular plants in a rainforest in the CNP and approach its implications for the handling and conservation of this protected area. Moreover, we collaborate to fill the knowledge gaps for mountain environments in Brazil. Our intent is to show that floristic listings of plant species are indispensable tools for biodiversity conservation and that they should be encouraged.

Materials and methods

Study area

The Caparaó National Park (CNP) is a protected area located between Espírito Santo and Minas Gerais states (Figure 1), within the Serra da Mantiqueira mountain range (20º18’ - 20º37’S and 41º42’ - 41º52’W). The park has 31,853.12 ha area, with 79% of being within the state of Espírito Santo (ICMBio 2015). It is located in the Atlantic Forest domain and protects different vegetation formations, such as montane forests (Dense Ombrophilous Forest and Semi-deciduous Seasonal Forest), high-altitude grasslands, and inselbergs (IBGE 2012, ICMBIO 2015, Couto et al. 2016COUTO, D.R., DIAS, H.M., PEREIRA, M.C.A., FRAGA, C.N. & PEZZOPANE, J.E.M. 2016. Vascular epiphytes on Pseudobombax (Malvaceae) in rocky outcrops (inselbergs) in Brazilian Atlantic Rainforest: basis for conservation of a threatened ecosystem. Rodriguesia 67(3): 583-601., Campos et al. 2018CAMPOS, P.V., VILLA, P.M., NUNES, J.A., SCHAEFER, C.E.R.G., POREMBSKI, S. & NERI, A.V. 2018. Plant diversity and community structure of Brazilian Páramos. J. Mt. Sci. 15(6): 1186-1198. doi: 10.1007/s11629-017-4674-7
https://doi.org/10.1007/s11629-017-4674-... ). The Dense Ombrophilous Forest are exclusive to the Espírito Santo state side of the Park.

Figure 1
Location map (a; b), relief representation (c), and pictures (d) of the Santa Marta valley, Caparaó National Park (PNC), Brazil. Photo: Araujo, E.A.

The CNP surrounding areas consist mostly of agricultural and cattle ranching, with emphasis on coffee and cattle farming, as well as a recent growth in areas destined to silviculture. Activities with potential negative impacts for the CNP are performed in surrounding areas, i.e. the use of pesticides, irregular deforestation for expanding agricultural areas (ICMBIO 2015). We also highlight anthropogenic pressures that may cause ecological unbalance in the park, such as unauthorized hunting, illegal extraction of palm hearts (Euterpe edulis Mart.), and the occurrence of forest fires (personal observation).

Floristic expeditions were concentrated in the Santa Marta valley (central point in the sampling area: 20º29’27,7’’S 41º45’15,6W), located in the municipality of Ibitirama - ES. The valley has an elevation range from 870 and 2480 m (Figure 1). Vegetation types reported to the area are Montane and Upper Montane Dense Ombrophilous Forests, according to the classification by IBGE (2012). The weather in the Ibitirama municipality is defined as Cwb according to the Köppen classification, adapted to Brazil by Alvares et al. (2013ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., DE MORAES GONÇALVES, J.L. & SPAROVEK, G. 2013. Köppen’s climate classification map for Brazil. Meteorol Z 22 (6): 711-728. doi: 10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0... ), being characterized as humid subtropical with dry winters and mild summers, and the region has annual precipitation of 1,284 mm and average annual temperatures of 16.8 ºC.

The vegetation in the beginning of the valley at lower elevation has different forest succession stages due to its wood extraction past, also presenting exotic/invading species (i.e. Eriobotrya japonica (Thunb.) Lindl.), representing one of the exotic species that exist inside the protected area (Field observation; not collected). The signs of anthropogenic activity are reduced throughout the valley, given that the vegetation is extremely preserved in the highest areas and with an observed great presence of epiphytes (personal observation).

1.2 Data collection

We performed botanic expeditions between 2012 and 2017 to collect specimens comprising all life forms in order to compose the floristic listing to the Santa Marta valley (CNP). We collected fertile plant samples along trails using the walk-over survey method (Filgueiras et al. 1994FILGUEIRAS, T.S., NOGUEIRA, P.E., BROCHADO, A.L. & GUALA, G.F. 1994. Caminhamento: um método expedito para levantamentos florísticos qualitativos. Cadernos de Geociências, 12, 39-43.), as well as samples in plots, covering an elevation gradient of around 700 m (900-1,600 m). We identified the species through pertinent literature as dichotomous keys of regional floras (e.g., Wanderley et al. 2005WANDERLEY, M. DAS G.L., SHEPHERD, G.J., MELHEM, T.S. & et al (eds). 2005. Flora fanerogâmica do estado de São Paulo. FAPESP, RiMa, São Paulo., 2012, Melhem et al. 2007MELHEM, T.S., WANDERLEY, M. DAS G.L., MARTINS, S.E. & et al. (eds). 2007. Flora fanerogâmica do estado de São Paulo. Instituto de Botânica, FAPESP, São Paulo, Martins et al. 2009MARTINS, S.E., WANDERLEY, M. DAS G.L., SHEPHERD, G.J. & et al. (eds). 2009. Flora fanerogâmica do estado de São Paulo. Instituto de Botânica, FAPESP, São Paulo.) and compared our materials to images available in virtual herbaria such as the Herbário Virtual - Reflora (http://reflora.jbrj.gov.br/reflora/herbarioVirtual/) and the Jabot (http://jabot.jbrj.gov.br/v2/consulta.php). Duplicates were sent to group experts at BHCB, CEPEC, HUFSJ, RB, SPSF, and UPCB herbaria - acronyms according to Thiers (2019THIERS, B. 2019. Index Herbariorum: A global directory of public herbaria and associated staff. Available from: http://sweetgum.nybg.org/science/ih/ (accessed 1 Jul 2018).
http://sweetgum.nybg.org/science/ih/... ) - for confirmation of the species. We have incorporated the specimens in the collection of the VIES and CAP Herbaria. In addition, sterile materials from plot sampling were included in the listing. These were reviewed by experts in their respective families and deposited in a didactic collection of CAP Herbaria. The exotic / invasive species were disregarded in this study. We try to keep a distance from the collection points of any area of human interference and therefore we prioritize including only native species.

Botanical families were classified according to the system proposed by the Angiosperm Phylogeny Group (APG IV 2016) for angiosperms, The Pteridophyte Phylogeny Group (2016) for ferns and lycophytes, and Christenhusz et al. (2011CHRISTENHUSZ, M.J.M., REVEAL, J.L., FARJON, A., GARDNER, R.R.M. & CHASE, M.W. 2011. A new classification and linear sequence of extant gymnosperms. Phytotaxa 19: 55-70. doi: 10.11646/phytotaxa.19.1.3
https://doi.org/10.11646/phytotaxa.19.1.... ) for gymnosperms. We confirmed name orthography, authorship and synonyms through consulting “Flora do Brasil” 2020 online (<http://floradobrasil.jbrj.gov.br/>), complementing it with data from the online platform of the Missouri Botanical Garden (http://www.tropicos.org) and The Plant List (http://www.theplantlist.org/).

Potentially threatened species were verified in the following lists: a) Red List of Espirito Santo state (Fraga et al. 2019FRAGA, C.N., PEIXOTO, A.L., LEITE, Y.L.R., SANTOS, N.D., OLIVEIRA, J.R.P.M., SYLVESTRE, L.S., SCHWARTSBURD, P.B., TULER, A.C., FREITAS, J., LÍRIO, E.J., COUTO, D.R., DUTRA, V.F., WAICHERT, C., SOBRINHO, T.G., HOSTIM-SILVA, M., FERREIRA, R.B., BÉRNILS, R.S., COSTA, L.P., CHAVES, F.G., FORMIGONI, M.H., SILVA, J.P., RIBEIRO, R.S., REIS, J.C.L., CAPELLÃO, R.T., LIMA, R.O., SAITER, F.Z. & et al. 2019. Lista da fauna e flora ameaçadas de extinção no estado do Espírito Santo. In: FRAGA, C.N., FORMIGONI, M.H. & CHAVES, F.G. (Orgs) Fauna e flora ameaçadas de extinção no estado do Espírito Santo. Santa Teresa, Instituto Nacional da Mata Atlântica, pp. 342-419.); b) Red List of Flora of Brazil/CNC Flora (Martinelli & Moraes 2013MARTINELLI, G. & MORAES, M.A. (eds). 2013. Livro vermelho da flora do Brasil. Andrea Jakobsson, Rio de Janeiro. 1100 p.; CNCFlora 2018); and c) The IUCN Red List of Threatened Species (IUCN 2017). New records of species from Espírito Santo state were compiled after the confirmation of group experts, as well as its verification in the database of the “Flora do Brasil” 2020 online (<http://floradobrasil.jbrj.gov.br/>) and Carrijo et al. (2020CARRIJO, T.T., ALVES-ARAÚJO, A.G., AMORIM, A.M.A., ANTAR, G.M., et al. 2020. Lista de espécies de plantas terrestres do Parque Nacional do Caparaó. In: Catálogo de Plantas das Unidades de Conservação do Brasil. Jardim Botânico do Rio de Janeiro. Disponible: [https://catalogo-ucs-brasil.jbrj.gov.br]. last acess in 29/jul/2020.
https://catalogo-ucs-brasil.jbrj.gov.br... ).

Results

We catalogued 361 species of vascular plants (Figure 2, Table 1) in the Santa Marta river valley, belonging to 78 botanical families (70 angiosperms and eight ferns and lycophytes), and 181 genera. The families with highest species richness were Melastomataceae (41 spp.) Lauraceae and Myrtaceae (30), Orchidaceae (26), Rubiaceae (24), Asteraceae (20), Piperaceae (15), Solanaceae (15) and Bromeliaceae (12), which altogether sum 59% of all compiled species. The most well represented genera regarding number of species were: Miconia (23 spp.), Ocotea (18), Myrcia (12), Psychotria (9), and Eugenia, Mikania, Peperomia and Leandra (8).

Figure 2
Sample of the vascular plants diversity collected in the Santa Marta valley, Caparaó National Park. (a) Psychotria bracteocardia (DC.) Müll.Arg. (Rubiaceae); (b) Clusia criuva Cambess. (Clusiaceae); (c) Aechmea coelestis (K.Koch) E.Morren (Bormeliaceae); (d) Psychotria nuda (Cham. & Schltdl.) Wawra (Rubiaceae); (e) Pleroma foveolatum (Naudin) Triana (Melastomataceae); (f) Scuticaria hadwenii (Lindl.) Planch. (Orchidaceae); (g) Schlumbergera cf. kautskyi (Horobin & McMillan) N.P.Taylor (Cactaceae); (h) Dryadella crenulata (Pabst) Luer (Orchidaceae); (i) Alstroemeria cunha Vell. (Alstroemeriaceae); (j) Peperomia urocarpa Fisch. & C.A.Mey. (Piperaceae); (k) Nematanthus crassifolius (Schott) Wiehler (Gesneriaceae); (l) Zygopetalum maxillare Lodd. (Orchidaceae); (m) Billbergia euphemiae E.Morren (Bromeliaceae); (n) Maxillaria caparaoensis Brade (Orchidaceae); (o) Athenaea martiana Sendtn. (Solanaceae); (p) Zygopetalum mackayi Hook. (Orchidaceae); (q) Staurogyne anigozanthus (Nees) Kuntze (Acanthaceae); (r) Pitcairnia flammea Lindl. (Bromeliaceae). Photos: Araujo, E.A.

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Table 1
List of vascular plant species collected in the Santa Marta valley Caparaó National Park, organized by group and plant family, scored for category of threat (DD = Data Deficient; LC = Least Concern; NT = Near Threatened; VU = Vulnerable; EN = Endangered; CR = Critically Endangered). * New records for the State of Espírito Santo; ** Possible new species that are under investigation. The acronym CAP (Herbarium “Capixaba”), where sterile specimens were deposited in a didactic collection, does not have a voucher number. The other with voucher were all deposited in herbaria VIES and CAP.

We found 3 new records for the State of Espírito Santo: Alsophila salvinii Hook. (Cyatheaceae); Pleroma foveolatum (Naudin) Triana; (Melastomataceae); Pilea hilariana Wedd. (Urticaceae), and three possible new species that are under investigation (Psychotria sp., Sloanea sp. and Solanum sp.), which are recent taxonomic discoveries and are being described.

Our results have also pointed out the existence of 43 species (12%) listed as threatened of extinction on The IUCN Red List of Threatened Species, in the Red Book of Brazilian Flora, and on the list of endangered flora species in the State of Espírito Santo (Table 1). The families that have the highest number of species categorized as threatened of extinction were: Myrtaceae (7 spp.), Lauraceae (6), Melastomataceae and Orchidaceae (5), Begoniaceae and Monimiaceae (4).

Based on our field observations during the inventory process, it was possible to notice a gradual change in the plant community throughout the valley (data on the ecology of plant communities are being published). To exemplify this differentiation, we observed some species occurring restrictedly at certain elevation, such as Alsophila setosa Kaulf., Cupania ludowigii Somner & Ferrucci, Euterpe edulis Mart. and Sorocea bonplandii (Baill.). W. C. Burger et al. that were only observed between approximately 1,100 m and 1,400 m of altitude, while species such as Baccharis oblongifolia (Ruiz & Pav.) Pers., Miconia longicuspis Cogn., M. molesta Cogn., and Weinmannia pinnata L. only occurred in elevations above 1,400 m. Some species were observed throughout the whole sampled altitude range, e.g., Alchornea triplinervia (Spreng.) Müll.Arg., Cyathea atrocastanea Labiack P.E. et Matos F.B., Dendropanax cuneatus (DC.) Decne. & Planch., Myrcia splendens (Sw.) DC., and Myrsine gardneriana A.DC. Species such as Bathysa australis (A.St-Hil.) K.Schum. and Leandra melastomoides Raddi mainly occurred in low elevations (1,000 m), especially in areas close to water streams. Maxillaria caparaoensis Brade is an endemic species to the CNP, with few sheets deposited in herbaria. Cyathea atrocastanea Labiack P.E. et Matos F.B. and Vochysia santaluciae M.C. Vianna & Fontella are endemic species of Espírito Santo, originally described for the Estação Biológica de Santa Lúcia in the Santa Teresa region.

Discussion

The new records for the state of Espírito Santo revealed in our study reflects the history of research efforts in certain places regarding the flora of the state (Carrijo et al. 2020CARRIJO, T.T., ALVES-ARAÚJO, A.G., AMORIM, A.M.A., ANTAR, G.M., et al. 2020. Lista de espécies de plantas terrestres do Parque Nacional do Caparaó. In: Catálogo de Plantas das Unidades de Conservação do Brasil. Jardim Botânico do Rio de Janeiro. Disponible: [https://catalogo-ucs-brasil.jbrj.gov.br]. last acess in 29/jul/2020.
https://catalogo-ucs-brasil.jbrj.gov.br... , Dutra et al. 2015DUTRA, V.F., ALVES-ARAÚJO, A. & CARRIJO, T.T. 2015. Angiosperm Checklist of Espírito Santo: using electronic tools to improve the knowledge of an Atlantic Forest biodiversity hotspot. Rodriguesia 66 (4): 1145-1152. doi: 10.1590/2175-7860201566414
https://doi.org/10.1590/2175-78602015664... , Araújo et al. 2018ARAÚJO, E.A., KUNZ, S.H., DIAS, H.M., CARRIJO, T.T. & ZORZANELLI, J.P.F. 2018. Inventários florísticos na região do Caparaó Capixaba revelam novos registros para a flora do Espírito Santo. Rodriguesia 69 (4): 1953-1963. doi: 10.1590/2175-7860201869429
https://doi.org/10.1590/2175-78602018694... ), especially for montane environments. Our data show that the Santa Marta Valley houses 20.2% (361 species) of the vascular plants from CNP (Carrijo et al. 2020), in addition our list includes 88 species of local flora not yet documented, representing an increase of approximately 1%. These knowledge gaps make it harder to map the species and biodiversity distribution correctly, and makes delimitation of endemic areas imprecise, being one of the main obstacles to obtain actual understanding and to establish proper plans for biodiversity conservation (Hopkins 2007HOPKINS, M.J.G. 2007. Modelling the known and unknown plant biodiversity of the Amazon Basin. J Biogeogr 34 (special issue):1400-1411. doi: 10.1111/j.1365-2699.2007.01737.x
https://doi.org/10.1111/j.1365-2699.2007... , Oliveira et al. 2016OLIVEIRA, U., PAGLIA, A.P., BRESCOVIT, A.D. & et al. 2016. The strong influence of collection bias on biodiversity knowledge shortfalls of Brazilian terrestrial biodiversity. Divers Distrib 22 (12): 1232-1244. doi: 10.1111/ddi.12489
https://doi.org/10.1111/ddi.12489... ). Our findings are relevant for contributing to filling this knowledge gap about the flora in the state, in addition to helping to reduce the current lack of knowledge on the biodiversity in certain locations within Brazilian protected areas (Oliveira et al. 2017).

We have also registered the third known occurrence of Freziera atlanticaZorzanelli & Amorim (Pentaphylacaceae). This specie was described in 2016ZORZANELLI, J.P.F., DIAS, H.M., DA SILVA, N.R. & KUNZ, S.H. 2016. Richness, structure and vegetation relationships of the woody layer in an upper montane forest in Caparaó National Park, Minas Gerais State, Brazil. Oecol Aust 20 (2): 177-183. doi: 10.4257/oeco.2016.2002.13
https://doi.org/10.4257/oeco.2016.2002.1... with samples collected in the Papuã Mountains-BA and in the Valentim Mountains-ES (Zorzanelli et al. 2016), given that these mountains belong to the surrounding areas of the Caparaó Mountains. We have also included a species for the recently described science, Myrcia altomontanaSobral & Zorzanelli (Myrtaceae) (Sobral et al. 2017SOBRAL, M., COSTA, I.G., SOUZA, M.C., ZORZANELLI, J.P.F. 2017. Five new species and one new combination in Brazilian Myrtaceae. Phytotaxa 307: 233-244. doi: 10.11646/phytotaxa.307.4.1
https://doi.org/10.11646/phytotaxa.307.4... ) in our list.

Plant communities of montane ecosystems usually present higher rates of endemism than ecosystems of lower elevations (Gentry 1995GENTRY, A.H. 1995. Patterns of diversity and floristic composition in Neotropical montane forests. In: CHURCHILL, S.P., BALSLEV, H., FORERO, E. & LUTEYN, J.L. (eds) Biodiversity and conservation of Neotropical montane forests. The New York Botanical Garden, New York, pp 103-126.), which makes the diversity in these places more vulnerable to climate change due to the specialization degree developed by the species colonizing these environments (Eller et al. 2015ELLER, C.B., BURGESS, S.S.O. & OLIVEIRA, R.S. 2015. Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae). Tree Physiol 35 (4): 387-399. doi: 10.1093/treephys/tpv001
https://doi.org/10.1093/treephys/tpv001... , 2016). Expanding knowledge on montane environments has been increasingly important as a support to avoid species loss (Bertoncello et al. 2011BERTONCELLO, R., YAMAMOTO, K., MEIRELES, L.D. & SHEPHERD, G.J. 2011. A phytogeographic analysis of cloud forests and other forest subtypes amidst the Atlantic forests in south and southeast Brazil. Biodivers Conserv 20: 3413-3433. doi: 10.1007/s10531-011-0129-6
https://doi.org/10.1007/s10531-011-0129-... ).

This list was performed in an area defined by the Brazilian government as priority for the conservation and with extremely high biological importance (MMA 2007). It is one of the first listings for vascular plants in forests above 1000 m in Espírito Santo state. Our results may thus contribute to real actions for the conservation of biodiversity in the park, given that listings are an important source of basic information for scientists and decision-makers (Ulloa Ulloa et al. 2017), in addition to providing relevant data for the “Flora do Espírito Santo” and “Catálogo de Plantas das Unidades de Conservação do Brasil” Projects (Dutra et al. 2015DUTRA, V.F., ALVES-ARAÚJO, A. & CARRIJO, T.T. 2015. Angiosperm Checklist of Espírito Santo: using electronic tools to improve the knowledge of an Atlantic Forest biodiversity hotspot. Rodriguesia 66 (4): 1145-1152. doi: 10.1590/2175-7860201566414
https://doi.org/10.1590/2175-78602015664... , Carrijo et al. 2020CARRIJO, T.T., ALVES-ARAÚJO, A.G., AMORIM, A.M.A., ANTAR, G.M., et al. 2020. Lista de espécies de plantas terrestres do Parque Nacional do Caparaó. In: Catálogo de Plantas das Unidades de Conservação do Brasil. Jardim Botânico do Rio de Janeiro. Disponible: [https://catalogo-ucs-brasil.jbrj.gov.br]. last acess in 29/jul/2020.
https://catalogo-ucs-brasil.jbrj.gov.br... ).

The CNP is one of the few large remnants in the Atlantic Forest, which thereby confers larger potential to keep high rates of biodiversity in relation to other smaller remnants, making it extremely important for species conservation (Oliveira et al. 2017OLIVEIRA, U., SOARES-FILHO, B.S., PAGLIA, A.P. & et al. 2017. Biodiversity conservation gaps in the Brazilian protected areas. Sci Rep-UK 7: 9141. doi: 10.1038/s41598-017-08707-2
https://doi.org/10.1038/s41598-017-08707... ). In a scenario in which protected areas within the Atlantic Forest are mostly small and disconnected (Joppa et al. 2008JOPPA, L.N., LOARIE, S.R. & PIMM, S.L. 2008. On the protection of “protected areas.” P Natl Acad Sci-Biol 105 (18): 6673-6678. doi: 10.1073/pnas.0802471105
https://doi.org/10.1073/pnas.0802471105... ), our list demonstrates the importance of CNP for the conservation of species, since one of the great challenges for biodiversity conservation in Brazil is to create matrices of protected areas which are large enough for the actual conservation of biological diversity (Rylands & Brandon 2005RYLANDS, A.B. & BRANDON, K. 2005. Brazilian protected areas. Conserv Biol 19 (3): 612-618. doi: 10.1111/j.1523-1739.2005.00711.x
https://doi.org/10.1111/j.1523-1739.2005... ).

We highlight herein the role played by the CNP in protecting species in montane environments of the Atlantic Forest, as shown in our study (Table 1). Protected areas are indeed the best strategy to reduce deforestation and the extinction of species in tropical regions (Joppa et al. 2008JOPPA, L.N., LOARIE, S.R. & PIMM, S.L. 2008. On the protection of “protected areas.” P Natl Acad Sci-Biol 105 (18): 6673-6678. doi: 10.1073/pnas.0802471105
https://doi.org/10.1073/pnas.0802471105... ). For example, a recent study in Brazil has demonstrated that protected areas preserve a considerable share of known Brazilian biodiversity (Oliveira et al. 2017OLIVEIRA, U., SOARES-FILHO, B.S., PAGLIA, A.P. & et al. 2017. Biodiversity conservation gaps in the Brazilian protected areas. Sci Rep-UK 7: 9141. doi: 10.1038/s41598-017-08707-2
https://doi.org/10.1038/s41598-017-08707... ).

However, we have mentioned the need for conservation actions that can surpass the CNP limits and to which the importance of local communities, should be recognized to protect forest remnants and maintain the biodiversity in these areas. It is important to have a positive interaction between the protected area and its surrounding areas, since the maintenance of native vegetation close to it contributes to maintaining ecological processes and species richness in protected areas (DeFries et al. 2005). In certain occasions, pressure within the protected area’s limits reflect the ones happening in its surrounding areas (Laurance et al. 2012LAURANCE, W.F., CAROLINA USECHE, D., RENDEIRO, J. & et al. 2012. Averting biodiversity collapse in tropical forest protected areas. Nature 489: 290-294. doi: 10.1038/nature11318
https://doi.org/10.1038/nature11318... ). Thus, affirmative actions taken with surrounding communities of the CNP are essential, aiming to reduce treats such illegal hunting and extraction of native species, especially endangered ones (e.g. E. edulis).

The botanical families that have presented the highest richness in our study are also the most rich ones across the Atlantic Forest mountains (Amorim et al. 2009AMORIM, A.M., JARDIM, J.G., LOPES, M.M.M., FIASCHI, P., BORGES, R.A.X., PERDIZ, R.O. & THOMAS, W.W. 2009. Angiospermas em remanescentes de floresta montana no sul da Bahia, Brasil. Biota Neotrop 9 (3): 313-348. doi: 10.1590/S1676-06032009000300028
https://doi.org/10.1590/S1676-0603200900... , Pifano et al. 2010PIFANO, D.S., VALENTE, A.S.M., ALMEIDA, H.D.S., MELO, P.H.A., CASTRO, R.M. & VAN DEN BERG, E. 2010. Caracterização florística e fitofisionômica da Serra do Condado, Minas Gerais, Brasil. Biota Neotrop 10 (1): 55-71. doi: 10.1590/S1676-06032010000100005
https://doi.org/10.1590/S1676-0603201000... , Coelho & Amorim 2014COELHO, M.M. & AMORIM, A.M. 2014. Floristic composition of the Montane Forest in the Almadina-Barro Preto axis, Southern Bahia, Brazil. Biota Neotrop 14: 1-41. doi: 10.1590/S1676-06033878
https://doi.org/10.1590/S1676-06033878... , Meireles et al. 2014MEIRELES, L.D., KINOSHITA, L.S. & SHEPHERD, G.J. 2014. Composição florística da vegetação altimontana do distrito de Monte Verde (Camanducaia, MG), Serra da Mantiqueira Meridional, Sudeste do Brasil. Rodriguesia 65 (4): 831-859. doi: 10.1590/2175-7860201465403
https://doi.org/10.1590/2175-78602014654... , BFG 2018, Dutra et al. 2015DUTRA, V.F., ALVES-ARAÚJO, A. & CARRIJO, T.T. 2015. Angiosperm Checklist of Espírito Santo: using electronic tools to improve the knowledge of an Atlantic Forest biodiversity hotspot. Rodriguesia 66 (4): 1145-1152. doi: 10.1590/2175-7860201566414
https://doi.org/10.1590/2175-78602015664... , Zorzanelli et al. 2017ZORZANELLI, J.P.F., DIAS, H.M., DA SILVA, A.G. & KUNZ, S.H. 2017. Vascular plant diversity in a Brazilian hotspot: floristic knowledge gaps and tools for conservation. Braz J Bot 40 (3): 819-827. doi: 10.1007/s40415-017-0386-z
https://doi.org/10.1007/s40415-017-0386-... ). In addition to these families, the most representative genera (Miconia) in our research usually present high numbers of species in montane and upper montane forests, being the main taxa in these formations (Oliveira-Filho & Fontes 2000). For example, Melastomataceae species are common to the Atlantic Forest, rainforests and more elevated forests (Goldenberg et al. 2012GOLDENBERG, R., BAUMGRATZ, J.F.A. & SOUZA, M.L.D.R. 2012. Taxonomia de Melastomataceae no Brasil: retrospectiva, perspectivas e chave de identificação para os gêneros. Rodriguesia 63 (1): 145-161. doi: 10.1590/S2175-78602012000100011
https://doi.org/10.1590/S2175-7860201200... ). We highlight the Miconia genus, represented in the Santa Marta Valley by almost half of known Miconia species known to Espírito Santo (23/55 spp. - 42%) (Bacci et al. 2016BACCI, L.F., CADDAH, M.K. & GOLDENBERG, R. 2016. The genus Miconia (Melastomataceae) in Espírito Santo, Brazil. Phytotaxa 271 (1): 1. doi: 10.11646/phytotaxa.271.1.1
https://doi.org/10.11646/phytotaxa.271.1... ). This number shows the significance of the elevation gradient for the wealth and abundance of plant groups, and also reinforces the need to consider it when proposing biodiversity conservation measures for mountains in the Atlantic Forest as center of diversity.

The occurrence of species classified into different endangered degrees enables a basis for conservation actions for these species. According to Moraes et al. (2014MORAES, M.A., BORGES, R.A.X., MARTINS, E.M., FERNANDES, R.A., MESSINA, T. & MARTINELLI, G. 2014. Categorizing threatened species: an analysis of the Red List of the flora of Brazil. Oryx 48 (2): 258-265. doi: 10.1017/S003060531200018X
https://doi.org/10.1017/S003060531200018... ), the conservation process of a species categorized as endangered begins with its inclusion on a Red List, and after that moment collective efforts must be made to protect these species. We suggest the adoption of the list of threatened species created by this study as a possibility to guide a better zoning of the park, subsidizing protection actions for the area as a whole.

Our results have indicated high diversity of vascular plants in the Santa Marta valley, municipality of Ibitirama, with presence of species threatened, new records, occurrence of possible new species and the presence of recently described species. These data contribute to the knowledge of the Caparaó National Park Flora, mainly for the Capixaba portion where further research to prospect biological data should be encouraged. Moreover, these results highlight the role played by protected areas, showing that they are an essential strategy for protecting diversity from to extinction threats. As such, the CNP plays an important role for species preservation in montane and upper montane forests in the Brazilian southeast and for biodiversity in the Atlantic rainforest, and efforts must be maintained to mitigate existing conflicts within the territorial limit of the protected area.

  • Ethics
    The authors declares that the research did not involve humans or clinical trials in this manuscript.
  • Data availability
    The authors inform that all data are available in the SISBIO Database because it was carried out within a federal protected area (National Park).

Acknowledgements

We thanks the numerous taxonomists associated to the BHCB, CEPEC, HUFSJ, RB, SPSF, UEC, and UPCB herbaria from different parts of the country for helping us to identify the collected material. List of experts who contributed to the identifications: Lycophytes and ferns: Alexandre Salino; Annonaceae: Adriana Quintella Lobão; Araliaceae: Pedro Fiaschi; Begoniaceae: Ludovic Kollmann; Bromeliaceae: Dayvid Rodrigues Couto and Talita Mota Machado; Clusiaceae: Lucas Marinho; Elaeocarpaceae: Daniela Sampaio; Gesneriaceae: Alain Chautems; Lauraceae: João Batista Baitello; Malpighiaceae: Cleiton Pessoa; Melastomataceae: Marcelo Reginato, Renato Goldenberg and Lucas Bacci; Monimiaceae and Siparunaceae: Elton John de Lírio; Myrtaceae: Marcos Sobral; Orchidaceae: Claudio Nicoletti de Fraga and Dayvid Rodrigues Couto; Pentaphylacaceae: João Paulo Fernandes Zorzanelli; Piperaceae: Valderes Sarnaglia Junior and Elsie Franklin Guimarães; Primulaceae: Tatiana Tavares Carrijo; Rubiaceae: Filipe Torres Leite; Leandro Giacomin; Vochysiaceae: Gustavo Shimizu. To Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq for the support through the Universal Public Call 14/2011 (475471/2011-3) and the Fundação de Amparo à Pesquisa e Inovação do Espírito Santo (FAPES) Universal Public Call no. 03/2017 (T.O.169 - SIAFEM: 80709605/18) for funding part of this research. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. To UFES for the logistic support, to Mr. Ademar Silva for climbing the trees to collect the evidence specimens, and to the many friends who have helped us in field collections. Finally, we want to thank the anonymous reviewer and the editor for their comment and advise that greatly improved the article.

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Publication Dates

  • Publication in this collection
    21 Dec 2020
  • Date of issue
    2021

History

  • Received
    20 Apr 2020
  • Reviewed
    22 Sept 2020
  • Accepted
    03 Nov 2020
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