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TREE COMMUNITY COMPOSITION AND ABOVEGROUND BIOMASS IN A SECONDARY ATLANTIC FOREST, SERRA DO MAR STATE PARK, SÃO PAULO, BRAZIL

COMPOSIÇÃO DA COMUNIDADE ARBÓREA E BIOMASSA AÉREA EM UMA FLORESTA ATLÂNTICA SECUNDÁRIA, PARQUE ESTADUAL DA SERRA DO MAR, SÃO PAULO, BRASIL

ABSTRAT

Projects involving floristic-phytosociological surveys are becoming increasingly frequent and is a very important tool to access the biodiversity, status of succession, biomass and carbon storage, guiding conservation and management strategies. These studies are particularly important in Atlantic Forest, which is considered a hotspot in terms of biodiversity, endemism and impacts. São Paulo State lost more than 80% of original forest and, nowadays, remains only isolated patches with a variety stage of succession and history of use. The aim of this study was to characterize the structure, composition and biomass of the woody plant community in a Montane Ombrophilous Dense Forest, Serra do Mar State Park. All trees with DBH ≥ 4.8 cm were sampled in 1 ha plot area, totaling 1,704 individuals belonging to 38 botanical families and 143 species. The highest species richness was found in the Myrtaceae and Lauraceae families, and the greatest value of abundance and Importance (IV) was observed in the Arecaceae and Euphorbiaceae. The Shannon index (H’) was 3.7 nats.ind.-1 and the Pielou’s evenness index (J) 0.7, characterizing a very diverse community with heterogeneous distribution of individuals by species. The aboveground biomass was 166.3 Mg.ha-1, similar to others studies in Atlantic forests. The forest composition, biomass and the history of land use indicate a middle secondary stage of regeneration, but evolving to a more mature condition.

Keywords:
Flux tower; Phytosociology; Serra do Mar State Park

RESUMO

Trabalhos envolvendo levantamentos florístico-fitossociológicos são cada vez mais frequentes e são uma ferramenta importante para acessar a biodiversidade, estágio de sucessão e acúmulo de biomassa e carbono, norteando estratégias de conservação e manejo. Esses estudos são particularmente importantes para a Mata Atlântica, considerada um hotspot em função da biodiversidade, endemismo e impactos. O Estado de São Paulo perdeu mais de 80% de sua floresta original e, atualmente, existem somente fragmentos isolados, com diferentes estágios de sucessão e histórico de uso. O objetivo desse estudo foi caracterizar a vegetação, a estrutura e a biomassa de um componente arbóreo localizado em Floresta Ombrófila Densa Montana, Parque Estadual da Serra do Mar. Foram amostrados indivíduos com DAP ≥ 4,8 cm em 1 ha, totalizando 1.704 indivíduos pertencentes a 38 famílias botânicas e 143 espécies. A maior riqueza de espécies foi encontrada nas famílias Myrtaceae e Lauraceae e a maior abundância e Valor de Importância (VI) em Arecaceae e Euphorbiaceae. O índice de Shannon (H’) foi de 3,7 nats.ind.-1 e a equabilidade de Pielou (J) 0,7, indicando que a comunidade da área é bastante diversa, contudo a distribuição dos indivíduos pelas espécies não é homogênea. A biomassa aérea foi de 166,3 Mg.ha-1, semelhante ao encontrado em outros estudos. A composição da floresta, biomassa e o histórico de exploração da área demonstraram que a fisionomia estudada apresenta-se em estádio secundário médio de regeneração avançando para uma condição mais tardia.

Palavras chave:
Torre de fluxo; Fitossociologia; Parque Estadual da Serra do Mar

INTRODUCTION

The Brazilian Atlantic Forest (AF) is the second largest tropical moist forest of South America, covering, initially, ca. 1.450 million km2 (17%) of the country (JOLY et al., 2014JOLY, C.A.; METZGER, J.P.; TABARELLI, M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytologist Tansley Review, v. 204, n.3, p. 459-473, 2014. ) and approximately 80% of the São Paulo State (JOLY et al., 1999JOLY, C.A.; AIDAR, M.P.M.; KLINK, C.A.; MCGRATH, D.G.; MOREIRA, A. G.; MOUTINHO, P.; NEPSTAD, D.C.; OLIVEIRA, A. A.; POTT, A.; RODAL, M.J.N.; SAMPAIO, E.V.S.B. Evolution of the Brazilian phytogeography classification systems: implications for biodiversity conservation. Ciência e Cultura, v. 51, n.5-6, p.331-348, 1999.). The Atlantic Forest is considered the oldest Brazilian forest (RIZZINI, 1997), characterized by its high biodiversity and endemism and a hotspot for biodiversity conservation (MYERS et al., 2000MYERS, N.; MITTERMEIER, R.A.; MITTERMEIER, C.G.; FONSECA, G.A.B.; KENT, J. Biodiversity hotspots for conservation priorities. Nature , v. 403, n. 6772, p. 853-858, 2000.), due land use change dating back to European’s settlement (RIBEIRO et al., 2009RIBEIRO, M.C.; METZGER, J.P.; MARTENSEN, A.C.; PONZONI, F.J.; HIROTA, M.M. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, v.142, n.6, p.1141-1153, 2009.). According to Malhi et al. (2014MALHI, Y.; GARDNER, T.A.; GOLDSMITH, G.R.; SILMAN, M.R.; ZELAZOWSKI, P. Tropical forests in the Anthropocene. Annual Review of Environment and Resources, v.39, p.125-159, 2014.), many human-modified tropical forest landscapes are complex and highly heterogeneous and must be better understood in order to develop efficient strategies for conservation.

In São Paulo State, only 15.3% of original forest cover remains (SOSMA/INPE, 2013SOSMA/INPE. Atlas dos remanescentes florestais da Mata Atlântica. Período 2011-2012. Relatório técnico. SOS Mata Atlântica e Instituto Nacional de Pesquisas Espaciais, 2013.). The majority of these remnants are found in the mountainous region of southeast near the shore, where is also located the largest Conservation Unit of the Atlantic Forest, the Serra do Mar State Park (GALINDO-LEAL; CÂMARA, 2005GALINDO-LEAL, C.; CÂMARA. I.G. Atlantic forest hotspots status: an overview. In: Mata Atlântica: biodiversidade, ameaças e perspectivas. Carlos Galindo-Leal, Ibsen de Gusmão Câmara (Ed.); traduzido por Edma Reis Lamas. - São Paulo: Fundação SOS Mata Atlântica - Belo Horizonte: Conservação Internacional, pp. 3-11, 2005. ). Nowadays, Atlantic Forest is mainly composed of isolated patches of small forests fragments, surrounded by pastures, agricultural fields and urbanization, and only few larger fragments remains (RIBEIRO et al., 2009RIBEIRO, M.C.; METZGER, J.P.; MARTENSEN, A.C.; PONZONI, F.J.; HIROTA, M.M. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, v.142, n.6, p.1141-1153, 2009.). Hobbs et al. (2009HOBBS, R.; HIGGS, E.; HARRIS, J. A. Novel ecosystems: implications for conservation and restoration. Trends in Ecology and Evolution, v.24, n.11, p.599-605, 2009.) highlighted that the effect of human activities in the forest and the surrounds could promote the development of new ecosystems which differ in composition and/or function from present and past systems, especially as a consequence of changing species distributions and environmental alteration. In the last three decades, many studies have been devoted to Atlantic forest, firstly focused in fauna and flora’s diversity and, more recently, focusing on the functionality of the forest and carbon stock (VIEIRA et al., 2008VIEIRA, S.A.; ALVES, L.F.; AIDAR, M.P.M.; ARAÚJO, L.S.; BAKER, T.; BATISTA, J.L.F.; CAMPOS, M.C.; CAMARGO, P.B.; CHAVE, J.; DELITTI, W.B.C.; HIGUCHI, N.; HONORIO, E.; JOLY, C.A.; KELLER, M.; MARTINELLI, L.A.; MATTOS, E.A.; METZKER, T.; PHILLIPS, O.; SANTOS, F.A.M.; SHIMABUKURO, M.T.; SILVEIRA, M.; TRUMBORE, S.E. Estimation of biomass and carbon stocks: the case of the Atlantic Forest. Biota Neotropica , v. 8, n. 2, 2008., JOLY et al., 2014JOLY, C.A.; METZGER, J.P.; TABARELLI, M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytologist Tansley Review, v. 204, n.3, p. 459-473, 2014. ).

The Brazilian Atlantic Forest comprises five main forest physiognomies - Dense Ombrophilous, Open Ombrophilous, Mixed Ombrophilous, Seasonal Semideciduous and Seasonal Deciduous Forests (JOLY et al., 2014JOLY, C.A.; METZGER, J.P.; TABARELLI, M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytologist Tansley Review, v. 204, n.3, p. 459-473, 2014. ). According to IBGE (2012)INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA/ IBGE. Manuais técnicos em geociências - Manual Técnico da Vegetação Brasileira. Rio de Janeiro, 271p. 2012., the dominant vegetation in the state of São Paulo is classified as Ombrophilous Dense Forest and its subdivisions based on altimetry. The one which covers the Serra do Mar and the Atlantic Plateau, with altitudes between 500 and 1,500 m, is classified as Montane Ombrophilous Dense Forest (Dm) and is partially protected by the Serra do Mar State Park (SMSP). This forest formation, composition, and functionality is strongly influenced by environmental conditions, especially rainfall, temperature and the frequency of fog (ALVES et al., 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.; VIEIRA et al., 2011VIEIRA, S.A.; ALVES, L.F.; DUARTE-NETO, P.J.; MARTINS, S.C.; VEIGA, L.G.; SCARANELLO, M.A.; PICOLLO, M.C.; CAMARGO, P.B.; CARMO, J.B.; SOUSA NETO, E.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Stocks of carbon and nitrogen and partitioning between above- and belowground pools in the Brazilian coastal Atlantic Forest elevation range. Ecology and Evolution, v.1, n.3, p.421-434, 2011.). The hillsides of Serra do Mar act as a moisture barrier against the sea breeze, which combined with the cold fronts and the South Atlantic Convergence Zone, resulting in an increase in precipitation rates, known as orographic rain (OLIVEIRA-FILHO; FONTES, 2000OLIVEIRA-FILHO, A.T.; FONTES, M.A.L. Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil, and the influence of climate. Biotropica, v.32, n.4b, p.793- 810, 2000.).

High altitudes environments, with colder and moister climates, tend to have lower temperatures and formation of mists and fog (BRUIJNZEEL; VENEKLAAS, 1998BRUIJNZEEL, L.A.; VENEKLAAS, E.J. Climatic conditions and Tropical Montane Forest productivity: the fog has not lifted yet. Ecology , v.79, n.1, p. 3-9, 1998.). Furthermore, these environmental conditions lead to the accumulation of large quantities of organic matter (SOETHE et al., 2008SOETHE, N.; LEHMANN, J.; ENGELS, C. Nutrient availability at different altitudes in a tropical montane forest in Ecuador. Journal of Tropical Ecology , v. 24, n. 04, p. 397-406, 2008.). In general, montane forests have higher density of individuals, lower diversity of species and families and, vascular and avascular epiphytic, compared with other tropical forests at lower altitudes (HAMILTON et al., 1995HAMILTON, L. S.; JUVIK, J. O.; SCATENA, F. N. (eds.) Tropical Montane Cloud Forests. Springer, New York, 1995.; LIEBERMAN et al., 1996LIEBERMAN, D.; LIEBERMAN, M.; PERALTA, R.; HARSHORN, E.G.S. Tropical forest structure and composition on a large-scale elevational gradient in Costa Rica. Journal of Ecology , v.84, p.137-152, 1996.). Alves et al. (2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.) found an increase of aboveground biomass along of altitudinal gradient in the Ombrophilous Dense Atlantic Forest, as well as litter accumulation and carbon and nitrogen stocks, both above and below ground (VIEIRA et al., 2011VIEIRA, S.A.; ALVES, L.F.; DUARTE-NETO, P.J.; MARTINS, S.C.; VEIGA, L.G.; SCARANELLO, M.A.; PICOLLO, M.C.; CAMARGO, P.B.; CARMO, J.B.; SOUSA NETO, E.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Stocks of carbon and nitrogen and partitioning between above- and belowground pools in the Brazilian coastal Atlantic Forest elevation range. Ecology and Evolution, v.1, n.3, p.421-434, 2011.). In the montane forests, the environmental conditions are imposed by higher altitude belts and theirs species could be more sensitive to current changes in the global climate, suggesting an evidence of biodiversity loss a near future (SILVA; TABARELLI, 2000SILVA, J.M.C; TABARELLI, M. Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature , v. 404, n. 6773, p. 72-74, 2000.).

Phytosociological analysis and estimation of biomass and carbon stock of a plant community are essential for ecological study, evaluation of successional status and useful for carbon flow measurements between the forest and the atmosphere, resulting from the balance between gain through photosynthesis and loss through respiration and mortality (KEELING; PHILLIPS, 2007KEELING, H.C.; PHILLIPS, O.L. The global relationship between forest productivity and biomass. Global Ecology and Biogeography, v. 16, n. 5, p.618-631, 2007.). Related to aboveground biomass, Melillo et al. (1993MELILLO, J.M.; MCGUIRE, A.D.; KICKLIGHTER, D.W.; MOORE, B.; VOROSMARTY, C.J.; SCHLOSS, A.L. Global climate change and terrestrial net primary production. Nature, v.363, n.6426, p.234-238, 1993.) suggested that the tropical forest has an important function on carbon exchange between atmosphere and terrestrial vegetation (36%), but there are still scarce data about the stock of carbon. Biomass and carbon stock can be calculated in a non-destructive manner by using allometric equations (CHAVE et al., 2005CHAVE, J.; ANDALO, C.; BROWN, S.; CAIRNS, M.; CHAMBERS, J.C.; EAMUS, D.; FÖLSTER, H.; FROMARD, F.; HIGUCHI, N.; KIRA, T.; LESCURE, J.; NELSON, B.W.; OGAWA, H.; PUIG, H.; RIÉRA, B.; YAMAKURA, T. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia, v.145, n.1, p.87-99, 2005.), which vary according to plant physiognomy. The total aboveground biomass is strongly influenced by the canopy height variation, wood density, and community plant composition, as well as successional stage of the forest, ecological interactions, climate and soil conditions (CHAVE et al., 2005; VIEIRA et al., 2008VIEIRA, S.A.; ALVES, L.F.; AIDAR, M.P.M.; ARAÚJO, L.S.; BAKER, T.; BATISTA, J.L.F.; CAMPOS, M.C.; CAMARGO, P.B.; CHAVE, J.; DELITTI, W.B.C.; HIGUCHI, N.; HONORIO, E.; JOLY, C.A.; KELLER, M.; MARTINELLI, L.A.; MATTOS, E.A.; METZKER, T.; PHILLIPS, O.; SANTOS, F.A.M.; SHIMABUKURO, M.T.; SILVEIRA, M.; TRUMBORE, S.E. Estimation of biomass and carbon stocks: the case of the Atlantic Forest. Biota Neotropica , v. 8, n. 2, 2008.; ALVES et al., 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.).

The main aim of this study was to characterize the tree species composition and aboveground biomass of a community located in the footprint area of an Eddy covariance flux tower (KLJUN et al., 2002KLJUN, N.; ROTACH, M.W.; SCHMID, H.P. A three-dimensional backward lagrangian footprint model for a wide range of boundary-layer stratifications. Boundary-Layer Meteorology, v.103, n.2, p.205-226, 2002.) in the Montane Ombrophilous Dense Forest, in the Santa Virginia Nucleus of Serra do Mar State Park. The plot studied had suffered clearcut for charcoal production more than 40 years ago, and since then, there is no more reported disturbance. This past disturbance influenced the observed ecological and biodiversity parameters. The long term carbon and water monitoring is fundamental for a better understanding of forest functionality, especially in Tropical Forests and climate change scenarios. In this aspect, the vegetation inventory is essential to characterize the plot status of succession and carbon flux, as plants are the largest biomass component in the ecosystem (FERSTER et al., 2015FERSTER, C. J.; TROFYMOW, J. A.; COOPS, N. C.; CHEN, B.; BLACK, T. A. Comparison of carbon-stock changes, eddycovariance carbon fluxes and model estimates in coastal Douglas-fir stands in British Columbia. Forest Ecosystems, v.2, n.1, p.13, 2015.).

MATERIAL AND METHODS

Study area

This study was carried out in Ribeirão da Casa de Pedra watershed -Santa Virgínia Nucleus, Serra do Mar State Park - Ubatuba, SP, more specifically in the footprint area of the flux tower installed in 2007 (23º19.506' S; 45º05.678' O; 1,020 m of altitude; http://www.fluxdata.org:8080/SitePages/siteInfo.aspx?BR-Afs - Figure 1). Santa Virgínia Nucleus at Serra do Mar State Park extending over an area of 17,000 hectares and altitude range from 740 to 1,600 m (INSTITUTO FLORESTAL, 2010INSTITUTO FLORESTAL . Unidades de Conservação do Estado de São Paulo. Disponível em: Disponível em: http://www.iflorestal.sp.gov.br/unidades_conservacao/index.asp . Acesso em 14 jan. 2010.
http://www.iflorestal.sp.gov.br/unidades...
) is considered an important area in biological and cultural aspects. Soils in the Serra do Mar State Park are classified as Inceptisol (USDA, 1999USDA. Soil Taxonomy: A Basic System of Soil Classification for Making and Interpreting Soil Surveys. United States Department of Agriculture, Natural Resources Conservation Service Agriculture. Handbook Number 436. 888p, 1999.) with approximately 60% of sand, 20% of silt and 20% of clay (Alves et al., 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.). Moreover, they are characterized by the presence of shallow soils, geologically ancient, well-drained, low pH, high phosphorus concentration and aluminum saturation compared to lower altimetric sites (SCARANELLO et al., 2011SCARANELLO, M.A.S.; ALVES, L.F.; VIEIRA, S.A.; CAMARGO, P.B.; JOLY, C.A.; MARTINELLI, L.A. Height-diameter relationships of tropical Atlantic moist forest trees in southeastern. Scientia Agricola, v. 69, n.1, p.26- 37, 2011.; MARTINS, 2010MARTINS, S.C. Caracterização dos solos e serapilheira ao longo do gradiente altitudinal da Mata Atlântica, estado de São Paulo. 2010 Tese de Doutorado. Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, 2010.).

FIGURE 1
Maps showing the location of the region (Ubatuba, SP) and study area in Santa Virgínia Nucleus - Serra do Mar State Park. The symbol (◊) indicate the sampled plot - Plot Torre (T).

The forest area is characterized by average litter accumulation of 7.2 Mg ha-1.yr-1, relatively well distributed along the year (AIDAR et al., unpublished data) in the surface layers of the soil, which also contains the largest nutritional reserves (VIEIRA et al., 2011VIEIRA, S.A.; ALVES, L.F.; DUARTE-NETO, P.J.; MARTINS, S.C.; VEIGA, L.G.; SCARANELLO, M.A.; PICOLLO, M.C.; CAMARGO, P.B.; CARMO, J.B.; SOUSA NETO, E.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Stocks of carbon and nitrogen and partitioning between above- and belowground pools in the Brazilian coastal Atlantic Forest elevation range. Ecology and Evolution, v.1, n.3, p.421-434, 2011.). According to Köppen (1948KÖPPEN, W. Climatologia: con un estudio de los climas de la tierra. México: Fondo de Cultura Economica, 478p, 1948.), the regional climate can be classified as Cwa - temperate and tropical climate, with hot and wet summers, and slightly dry winters. The average minimum temperature is 10.6 °C, the maximum of 26.1 °C (MARTINS, 2010MARTINS, S.C. Caracterização dos solos e serapilheira ao longo do gradiente altitudinal da Mata Atlântica, estado de São Paulo. 2010 Tese de Doutorado. Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, SP, 2010.) and the average annual rainfall of 2,200 mm with the wettest months being December, January and February (SIEGLOCH; FROEHLICH; SPIES, 2012SIEGLOCH, A.E.; FROEHLICH, C.G; SPIES, M.R. Diversity of Ephemeroptera (Insecta) of the Serra da Mantiqueira and Serra do Mar, southeastern Brazil. Revista Brasileira de Entomologia, v.56, n.4, p.473-480, 2012.).

Veloso et al. (1991VELOSO, H.P.; RANGEL-FILHO, A.L.R.; LIMA, J.C. Classificação da vegetação brasileira adaptada a um sistema universal. IBGE. Rio de Janeiro, 1991.) classified the vegetation in the plot area as Montane Ombrophilous Dense Forest. Tabarelli and Mantovani (1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.) reported that as a result of land occupation and logging activities in the 1960´s, the current forest vegetation is a mosaic with different successional stages (primary and secondary), pastures and Eucalyptus spp. plantations. Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.) found a physiognomy composed by large trees and uniform canopy covering 80% of the Ribeirão da Casa de Pedra watershed in Santa Virginia Nucleus.

Vegetation Sampling

The phytosociological survey was performed using the plot method (MUELLER-DOMBOIS; ELLENBERG, 1974MUELLER-DOMBOIS, D.; ELLENBERG, H. Aims and methods of vegetation ecology. John Wiley and Sons, New York, p. 44-66,1974.). The sampling site is located in the flux tower footprint at 1,020 m of altitude. The 100 x100 m (1 ha) plot was divided into 25 blocks of 20 x 20 m. All living trees with stem diameter (one or multiple) at 1.30 m above the ground (DBH) ≥ 4.8 cm were included in the sample. The approximate height (from the base to the highest branch) was acquired either with a clinometer or by comparison with known height, to define the average height. The plant material was collected in the reproductive or vegetative stage (FIDALGO; BONONI, 1984FIDALGO, O.; BONONI, V.L.R. Técnicas de coleta, preservação e herborização de material botânico. Manual 4. Instituto de Botânica, São Paulo, 1984.) and identified by using a specialized bibliography and comparisons with specimens deposited in herbarium collections from São Paulo (“SPSF - Instituto FlorestalINSTITUTO FLORESTAL. Plano de Manejo do Parque Estadual da Serra do Mar. São Paulo, 2006.”) and Campinas (“UEC - Universidade Estadual de Campinas”). The floristic list was prepared according to the classification system proposed in APG III (2009)ANGIOSPERM PHYLOGENY GROUP/APG. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society, v.161, p.105-121, 2009., and the confirmation and updating of species names and authors were accomplished by consulting the REFLORA - Flora do Brasil 2020 - LEFB database (FLORA DO BRASIL 2020FLORA DO BRASIL 2020. Jardim Botânico do Rio de Janeiro. Disponível em: < Disponível em: http://floradobrasil.jbrj.gov.br/ >. Acesso em: 30 Mai. 2016
http://floradobrasil.jbrj.gov.br/...
, 2016). Materials with flowers, fruit, or vegetative were incorporated into the UEC Herbarium of the University of Campinas and the codes of the incorporated exsiccates can be found on the Herbarium of the State University of Campinas (UEC) available in the speciesLink Project (CRIA, 2016CRIA. Centro de Referência em Informação Ambiental - speciesLink. http://splink.cria.org.br/ (Access in March/2016).
http://splink.cria.org.br/...
).

Estimates of the vegetation aboveground biomass (AGB) were carried out to complement the characterization of the study area and it is an useful knowledge to evaluate the carbon fluxes between aboveground forest ecosystems and the atmosphere (CHAVE et al., 2005CHAVE, J.; ANDALO, C.; BROWN, S.; CAIRNS, M.; CHAMBERS, J.C.; EAMUS, D.; FÖLSTER, H.; FROMARD, F.; HIGUCHI, N.; KIRA, T.; LESCURE, J.; NELSON, B.W.; OGAWA, H.; PUIG, H.; RIÉRA, B.; YAMAKURA, T. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia, v.145, n.1, p.87-99, 2005.). The model chosen for moist forest stands was based on Chave et al. (2005CHAVE, J.; ANDALO, C.; BROWN, S.; CAIRNS, M.; CHAMBERS, J.C.; EAMUS, D.; FÖLSTER, H.; FROMARD, F.; HIGUCHI, N.; KIRA, T.; LESCURE, J.; NELSON, B.W.; OGAWA, H.; PUIG, H.; RIÉRA, B.; YAMAKURA, T. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia, v.145, n.1, p.87-99, 2005.), the same employed by Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.) in other plot at Serra do Mar State Park (Equation 1). The wood density values were extracted from Chave et al. (2006)CHAVE, J.; MULLER-LANDAU, H. C.; BAKER, T. R.; EASDALE, T. A.; TER STEEGE, H., WEBB, C. O. Regional and phylogenetic variation of wood density across 2456 neotropical tree species. Ecological Applications, v.16, n. 6, p.2356-2367, 2006., when it was not available for one specific species, it was used the average of the genus or family. The allometric equations for palm trees (Equation 2) and ferns (Equation 3) were based on other authors (NASCIMENTO; LAURANCE, 2002NASCIMENTO, H.E.M.; LAURENCE, W.F. Total aboveground biomass in central Amazonian rainforests: a landscape-scale study. Forest Ecology and Management , v. 168, n. 1, p. 311-321, 2002.; TIEPOLO et al., 2002TIEPOLO, G.; CALMON, M.; FERETTI, A.R. Measuring and monitoring carbon stocks at the Guaraqueçaba climate action project, Paraná, Brazil. In: K. Lin and J. Lin (eds.) International Symposium on Forest Carbon Sequestration and Monitoring . Extension Series TFRI, v.153, p.98-115, 2002., respectively). Lianas, bamboos, and epiphytes were not included. Where, = wood specific density (g.cm-3) (CHAVE et al. 2006, ALVES et al. 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.), DBH = diameter at 1.30 m height from the ground (cm), H = height (m), exp = exponent applied to the base, ln = natural logarithm.

A G B = e x p [ 2.977 + l n ( ρ . D B H 2 . H ) ] (1)

A G B = { e x p [ 0.9285 . l n ( D B H 2 ) + 5.7236 ] . 1.05001 } . 10 - 3 (2)

A G B = 4266348 . { 1 [ 2792284 . e x p ( 0.313677 . H ) ] } - 1 (3)

Data Analysis

Stem density, absolute and relative dominance (Basal area), absolute and relative frequency, importance, coverage and diversity (Shannon’s diversity, H’; Pielou’s evenness, J) indexes were calculated using FITOPAC 2.1 software (SHEPHERD, 2010SHEPHERD, G.J. FITOPAC 2.1. Campinas, 2010.; PIELOU, 1975PIELOU, E.C. Ecological diversity. John Wiley and Sons, New York, 1975.). Individuals were grouped by diameter and height classes to evaluate the forest structure. In addition, the species were classified into the successional groups proposed by Gandolfi et al. (1995GANDOLFI, S.; LEITÃO FILHO, H.; BEZERRA, C. L. F. Levantamento Florístico e caráter sucessional das espécies arbustivo-arbóreas de uma Floresta Mesófila Semidecídua no município de Guarulhos, SP. Brazilian Journal of Botany, v.55, n.4, p.753-767, 1995.), especially considering the survival and germination in the light, as pioneer, early secondary and late secondary. Comparisons with the literature (AIDAR et al., 2003AIDAR, M.P.M.; SCHMIDT, S.; MOSS, G, STEWART, G.R.; JOLY, C.A. Nitrogen use strategies of neotropical rainforest trees in threatened Atlantic Forest. Plant Cell and Environment, v. 26, n.3, p.389-399, 2003.; GOMES et al., 2011GOMES, J.A.M.A.; BERNACCI, L.C.; JOLY, C.A. Diferenças florísticas e estruturais entre duas cotas altiduninais da Floresta Ombrófila Densa Submontana Atlântica, do Parque Estadual da Serra do Mar, município de Ubatuba/SP, Brasil. Biota Neotropica, v.11, n.2, 2011. ; MEDEIROS AND AIDAR, 2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.; PADGURSCHI et al., 2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.) were used for the species definition in each of the ecological groups.

RESULTS AND DISCUSSION

Of a total of 1,704 trees found, 1,596 (93.7 %) were identified, 75 (4.4%) were unidentified and 33 (1.9%) correspond to standing dead individuals. The identified individual trees were distributed in 143 species belonging to 38 botanical families (Table 1 and 2), including 258 palms (Euterpe edulis - Arecaceae) and 117 ferns represented by Cyatheaceae family.

Table 1
List of 20 most important species, families and phytosociological parameters in Montane Ombrophilous Dense Forest, Serra do Mar State Park. NInd - Number of individuals, RelDe - Relative density, RelFr - Relative frequency, IV - Importance value, CV - Coverage value, SG. - Successional group (PI - Pioneer, ES - Early secondary, LS - Late secondary and NC - Not characterized).

Table 2
List of species, families and phytosociological parameters in the Montane Ombrophilous Dense Forest, Serra do Mar State Park. NInd - Number of individuals, RelDe - Relative density, RelFr - Relative frequency, IV - Importance value, CV - Coverage value, SG. - Successional group (PI - Pioneer, ES - Early secondary, LS - Late secondary and NC - Not characterized).

The average and maximum values of diameter were 12.8 cm and 108.2 cm, respectively. The maximum height were 35.5 m and average of 10.3 m. Stem density values (1,704 ind.ha-1) and basal area (31.9 m2.ha-1) were similar to those found in other studies also developed in the area (MEDEIROS; AIDAR, 2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.; ALVES et al., 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.; PADGURSCHI et al., 2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.). Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.), in a Montane Ombrophilous Dense Forest community of with more than 35 years of regeneration, found 1,743.3 ind.ha-1 and basal area of 28.5 m2.ha-1, whereas Tabarelli and Mantovani (1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.) in other patch of 40-year forest at 870 m to 1.100 m obtained 2,735 ind.ha-1 and 33.4 ind.ha-1. Joly et al. (2012JOLY, C.A.; ASSIS, M.A.; BERNACCI, L.C.; TAMASHIRO, J.Y.; CAMPOS, M.C.R.; GOMES, J.A.M.A.; LACERDA, M.S.; SANTOS, F.A.M.; PEDRONI, F.; PEREIRA, L.S. et al. Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotropica , v.12, n. 1, p.125-145, 2012. ) compared all permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil and obtained 1,965 stems.ha-1 in a mature and preserved plot at Santa Virginia Nucleus, with higher percentage of palms compared to others phytophisiognomies. Lieberman et al. (1996LIEBERMAN, D.; LIEBERMAN, M.; PERALTA, R.; HARSHORN, E.G.S. Tropical forest structure and composition on a large-scale elevational gradient in Costa Rica. Journal of Ecology , v.84, p.137-152, 1996.) highlighted a positive relationship between tree density and altitude at Atlantic Forest and other tropical forests.

The Shannon diversity index H’ = 3.7 nats.ind.-1 and the evenness index J’ = 0.7, demonstrated that the community is diverse, but with uneven distribution of individuals by species, including species with a great number of individuals and species with only one representative. Other plots at Santa Virgínia Nucleus, located in different areas and with distinct historical use, showed similar indexes values as found in this study (both with H’ = 3.6 nats.ind.-1 and J = 0.7) (PADGURSCHI et al., 2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.; MEDEIROS; AIDAR, 2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011. ). Padgurschi et al. (2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.) compared two plots with different history of human impact within the Serra do Mar State Park regarding to the floristic composition, forest structure and aboveground biomass, and they found lower biodiversity in the plot that suffered selective logging 40 years ago in comparison to the undisturbed site (H’= 3.72 nats.ind.-1, J = 0.7 and H’ = 4,05 nats.ind.-1, J = 0.8, respectively; reduction in 40 tree species). Considering altitude, sites located in lower altitudes showed higher Shannon’s diversity indexes (348 e 395 m altitude - H’ = 4.5 nats.ind.-1 - ROCHELLE et al., 2011ROCHELLE, A.L.C.; CIELO-FILHO, R.; MARTINS, F.R. Tree community structure in an Atlantic forest fragment at Serra do Mar State Park, southeastern Brazil. Biota Neotropica , v.11, n.2, p. 337-346,2011.) and confirmed the hypothesis that there is a trend to the reduction in diversity with the increased altitude, since the environmental conditions imposed by higher altitudes, such as temperature reduction, frequent fog’s events and high rates of precipitation, could limit the occurrence of some species and reduce the diversity indexes (TABARELLI; MANTOVANI, 1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.).

The families’ dominance (basal area) in the study area, especially Arecaceae, Cyatheaceae, Fabaceae, Lauraceae, Myrtaceae and Rubiaceae were similar to the results obtained by Tabarelli and Mantovani (1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.), Padgurschi et al. (2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.), Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.) and Joly et al. (2012JOLY, C.A.; ASSIS, M.A.; BERNACCI, L.C.; TAMASHIRO, J.Y.; CAMPOS, M.C.R.; GOMES, J.A.M.A.; LACERDA, M.S.; SANTOS, F.A.M.; PEDRONI, F.; PEREIRA, L.S. et al. Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotropica , v.12, n. 1, p.125-145, 2012. ). Peixoto and Gentry (1990PEIXOTO, A.L.; GENTRY, A. Diversidade e composição florística da mata de tabuleiro na Reserva Florestal de Linhares (Espírito Santo. Brasil). Revista Brasileira de Botânica, v.13, n.1, p.19-25, 1990.) pointed that Myrtaceae and Lauraceae families predominate in forest formations along the entire Atlantic coast, especially under the influence of fog or in the montane forests. The sum of these families resulted in approximately 54% of the individuals present in the sampling area and influenced the importance value and coverage value results. They are often found in Atlantic Forest, especially in montane formations, along with a low number of woody vines and a high abundance of epiphytes, ferns and bamboos (JOLY et al., 2014JOLY, C.A.; METZGER, J.P.; TABARELLI, M. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytologist Tansley Review, v. 204, n.3, p. 459-473, 2014. ; 2012). The presence of the Monimiaceae family with 52 individuals and nine species, confirms the hypothesis of Peixoto (1987PEIXOTO, A.L. Revisão taxonômica do gênero Mollinedia Ruiz et Pavon (Monimiaceae, Monimioideae). 1987 Tese de Doutorado, Universidade Estadual de Campinas, Campinas, 1987.) and Padgurschi (2010), which observed the same species in a near plot at montane Forests in Serra do Mar State Park. In fact, there are many species similarities between this study and the Padgurschi et al. (2011): Firstly, both had experienced a disruption for over 40 years ago and; secondly, both showed abundance of recognizable secondary species, like Inga spp., Miconia spp. and Alchornea triplinervia.

The Arecaceae family was represented only by Euterpe edulis, as also found by Padgurschi et al. (2011PADGURSCHI, M.C.G.; PEREIRA, L.S.; TAMASHIRO, J.Y.; JOLY, C.A. Composição e similaridade florística entre duas áreas de Floresta Atlântica Montana, São Paulo, Brasil. Biota Neotropica , v.11, n.2, p.00-00, 2011.) and Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.). Joly et al. (2012JOLY, C.A.; ASSIS, M.A.; BERNACCI, L.C.; TAMASHIRO, J.Y.; CAMPOS, M.C.R.; GOMES, J.A.M.A.; LACERDA, M.S.; SANTOS, F.A.M.; PEDRONI, F.; PEREIRA, L.S. et al. Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotropica , v.12, n. 1, p.125-145, 2012. ) highlighted the increase of palm species in higher altitudes, reaching more than 400 ind.ha-1 in the Montane Ombrophilous Dense Forest, as well as Cyatheaceae species. In the studied plot, Cyatheaceae family prevailed in the lower parts of the hillside, while the Arecaceae individuals had wider distribution throughout the plot. The distribution pattern suggest that these species could be potential competitors as they both have similar architecture, form dense populations in mountainous regions and usually share similar habitats (TRYON; TRYON, 1982TRYON, R. M.; TRYON, A. F. Ferns and allied plants with special reference to tropical America. Springer Verlag, New York, 1982.).

The distribution of all live trees into diameter classes showed an exponential negative or unbalanced inverted J-shaped curve, i.e., there was a predominance of young individuals in early regeneration stages and lower values of diameter and a marked decrease in the larger classes (Figure 2). The first two classes (DHB up to 20 cm) contained about 86% of the individuals sampled, followed by the classes with DHB up to 40cm with 12%, and the other classes with the remaining 2% of the total individuals. The average diameter for the entire sample was 12.8 cm, with the highest value from an Alchornea triplinervia (108.3 cm) individual.

FIGURE 2
Distribution of individuals in their respective diameter classes (in centimeters) at Santa Virgínia Nucleus.

The individual distribution by height classes (Figure 3) showed low overall height with an average of 10.3 m, a result similar to other studies developed in the Atlantic Forest (OGATA; GOMES, 2006OGATA, H.; GOMES, E.P.C. Estrutura e composição da vegetação no Parque CEMUCAM, Cotia, SP. Hoehnea , v.33, n.3, p.371-384, 2006.; MEDEIROS; AIDAR, 2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.; JOLY et al., 2012JOLY, C.A.; ASSIS, M.A.; BERNACCI, L.C.; TAMASHIRO, J.Y.; CAMPOS, M.C.R.; GOMES, J.A.M.A.; LACERDA, M.S.; SANTOS, F.A.M.; PEDRONI, F.; PEREIRA, L.S. et al. Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotropica , v.12, n. 1, p.125-145, 2012. ). Most individuals (74%) showed heights between 6-16 m, however, less than 5% of individuals have heights between 18-26 m, similar to results of Joly et al. (2012JOLY, C.A.; ASSIS, M.A.; BERNACCI, L.C.; TAMASHIRO, J.Y.; CAMPOS, M.C.R.; GOMES, J.A.M.A.; LACERDA, M.S.; SANTOS, F.A.M.; PEDRONI, F.; PEREIRA, L.S. et al. Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradient in southeastern Brazil. Biota Neotropica , v.12, n. 1, p.125-145, 2012. ). The taller individuals are members of the Araliaceae, Chrysobalanaceae, Elaeocarpaceae, Euphorbiaceae, Fabaceae, Lauraceae, Melastomataceae, Myrtaceae and Phyllanthaceae families. They could form an emergent canopy and are, mainly, classified as early and late secondary in the succession. Moreover, representatives of the Cyatheaceae and Arecaceae (E. edulis) families are typical of the understory of a forest, reaching average of 5.3 and 10.9 m high. The understanding of stem diameter and height represent the growth and, consequently, the forest structure and biomass (COOMES; ALLEN, 2007COOMES, D.A.; ALLEN, R.B. Effects of size, competition and altitude on tree growth. Journal of Ecology , v.95, p.1084-1097, 2007.).

FIGURE 3
Distribution of individuals in size classes (height in meters) at Santa Virginia Nucleus. The y-axis represents the number of individuals.

The environmental conditions vary along altitudinal gradients. At higher altitudes, the low-level clouds and fog formation could reduce the annual irradiance (SOUSA NETO et al., 2011SOUSA NETO, E.; CARMO, J.B.; KELLER, M.; MARTINS, S.C.; ALVES, L.F.; VIEIRA, S.A.; PICCOLO, M.C.; CAMARGO, P.; COUTO, H.T.Z.; JOLY, C.A.; MARTINELLI, L.A. Soil-atmosphere exchange of nitrous oxide, methane and carbon dioxide in a gradient of elevation in the coastal Brazilian Atlantic forest. Biogeosciences, n.8, p.733-742, 2011.). This condition, associated with the reduction of the air and soil temperature and prevalence of strong winds, could be the cause of the decrease in tree heights and the increase in diameter in montane forests (ALVES et al., 2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.). Also, the distribution of light is more asymmetric in steeper terrain (ALVES et al., 2010), resulting in individuals shorter, with larger diameters instead of height, and wider crowns (ALVES; SANTOS, 2002ALVES, L.F.; SANTOS, F.A.M. Tree allometry and crown shape of four tree species in Atlantic rain forest, southeast Brazilian. Journal of Tropical Ecology, v.18, n. 2, p.245-260, 2002.).

According to the successional classification, the group “Not characterized (NC)” is composed of 20 species (14%), “Pioneer (PI)” by 14 species (9.8%), “Early secondary (ES)” by 32 species (22.4%) and “Late secondary (LS)” 77 species (54%) (Figure 4A). Guariguata and Ostertag (2001GUARIGUATA, M.R.; OSTERTAG, R. Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management , v.148, n.1, p.185-206, 2001. ) assumed that forests at early stages are mainly influenced by factors that guide colonization, related to germination and sprouts. In contrast to later stages, when biotic and abiotic competitive ability and tolerance of environmental conditions among species (determined primarily by rates of species-specific growth, longevity, maximum size at maturity and the degree of shade tolerance) largely dictate patterns of species replacement over time. The level of succession also contributes to nitrogen fertilization of the soil, carbon accumulation in biomass, composition of species and stem density (KOERSELMAN; MEULEMAN, 1996KOERSELMAN, W.; MEULEMAN, A.F.M. The vegetation N : P ratio: a new tool to detect the nature of nutrient limitation. Journal of Applied Ecology , v.33, p.1441-1450, 1996.). Due to the evolution in succession, gaps suitable for the light demanding species tend to be rare, decreasing the number of pioneer species (DENSLOW, 1980DENSLOW, J.S. Patterns of plant species diversity during succession under different disturbance regimes. Oecologia , v.46, n.1, p.18-21, 1980.), while Finegan (1996FINEGAN, B. Pattern and process in neotropical secondary rain forests: the first 100 years of succession. Tree, v.11, n.3, p.119-124, 1996.) pointed that the proximity to a mature forest could improve the capacity of a secondary area to regenerate, especially because of the seed rain, remnant trees, pollinators, and dispersers.

FIGURE 4
Distribution of species and individuals in their respective successional groups at Santa Virgínia Nucleus. Figure “A” represents number of species and “B” individuals. NC - not characterized, PI - pioneers, ES - early secondary and ST - late secondary. The y-axis represents the number of species (A) e individuals (B).

The abundance of early secondary individuals (853 ind.) (Figure 4B), the presence of species considered typical of disturbed environments, such as Vernonia sp.1, Alchornea triplinervia, Hyeronima alchorneoides and Casearia decandra, the land use history, presence of gaps and several bamboo clumps suggest that the studied area is secondary with more than 40 years of succession (TABARELLI; MANTOVANI, 1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.). However, species diversity and abundance of individuals (575) from the late secondary category suggest that the initial phase of regeneration is progressing toward the climax condition. The diversity of species from Myrtaceae and Lauraceae families indicate a progress in the succession, although the abundance of Alchornea triplinervia has reinforced the classification in middle secondary stage (TABARELLI; MANTOVANI, 1999). This information is highly significant to a better understanding of the community’s gas exchange potential around the flux tower (FREITAS, 2012FREITAS, H.C. A influência dos transportes advectivos na estimativa do fluxo líquido do ecossistema: um estudo de caso para a Mata Atlântica com uso de técnicas micrometeorológicas. Tese de Doutorado - Escola Superior de Agricultura “Luiz de Queiroz”, USP, Piracicaba. 84p., 2012.), as secondary forests show normally high productivity and biomass accumulation pattern when compared with mature forests (BROWN; LUGO, 1990BROWN, S.; LUGO, A. E. Tropical secondary forests. Journal of Tropical. Ecology, v. 6, n.1, p.1- 32, 1990.).

The inverted J-shaped standard of diameter classes is common in tropical forests with a diversity of age and composition, also found in Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.). It represents the age distribution of a community, since there is a direct relationship between the increase in the diameter and the age of the plant (OLIVER; LARSON, 1996OLIVER, C.D.; LARSON, B.C. Forest stand dynamics. John Wiley and Sons. New York, 1996.). Furthermore, it indicates a self-regeneration within the community, with a predominance of recruited individuals with lower diameter values (SILVA; NASCIMENTO, 2001SILVA, G.C.; NASCIMENTO, M.T. Fitossociologia de um remanescente de mata sobre tabuleiros no norte do estado do Rio de Janeiro (Mata do Carvão). Brazilian Journal of Botany , v.24, n.1, p.51-62, 2001.). The difference between the frequencies of individuals in the first and the last classes indicates that the life cycle was blocked by some past event, such as the selective cutting of larger trees (NEVES; PEIXOTO, 2008NEVES, G.M.S.; PEIXOTO, A.L. Florística e estrutura da comunidade Arbustivo-arbórea de dois remanescentes em regeneração de floresta atlântica secundária na reserva biológica de Poço das Antas, Silva Jardim, Rio de Janeiro. São Leopoldo: Instituto Anchietano de Pesquisas. Pesquisas, botânica, v.59, p.71-112, 2008. ) and could reinforce the successional status of the area as middle secondary.

The calculations of the aboveground biomass using allometric models indicated that the biomass accumulated was of 166.3 Mg.ha-1, with tree species representing the greatest amount of biomass (155.6 Mg.ha-1 or 93.6%), followed by the palm trees (9.2 Mg.ha-1 or 5.5%) and the ferns (1.5 Mg.ha-1 or 0.9%). The biomass at Montane Ombrophilous Dense Forest in the study of Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.) was similar to this study, 189.2 Mg.ha-1. The slightly higher result may be due to extrapolation errors, since the area sampled by these authors was of 0.2 ha and the result was estimated for 1 ha, unlike in the present study where exactly 1 ha of forest was surveyed. Padgurschi (2010PADGURSCHI, M.C.G. Composição e estrutura arbórea de um trecho de Floresta Ombrófila Densa Montana com taquaras na Mata Atlântica. 2010 Dissertação de Mestrado. Universidade Estadual de Campinas, Campinas, SP, 2010.) and Alves et al. (2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.) obtained higher montane forest biomass results in mature forest, 282.6 Mg.ha-1 and 271.7 Mg.ha-1, respectively. As we propose that the studied area is evolving from a logged to a late secondary forest, the aboveground biomass also has the tendency to increase with time, when species with higher values of wood density and the basal area would influence it (HOUGHTON et al., 2009HOUGHTON, R.A.; HALL, F.; GOETZ, S.J. Importance of biomass in the global carbon cycle. Journal of Geophysical Research, v. 114, n. G2, 2009.).

Structure, composition, and function are the three essential attributes of forest ecosystems. Mandal and Joshi (2014MANDAL, G.; JOSHI, S.P. Analysis of vegetation dynamics and phytodiversity from three dry deciduous forests of Doon Valley, Western Himalaya, India. Journal of Asia-Pacific Biodiversity, v.7, n.3, p.292-304, 2014.) suggested that these characteristics could change in response to climate, topography, soil and disturbances. The aboveground live biomass varies widely in neotropical forests due to regional differences in the individual size, wood density, species composition, soil fertility, topography and disturbance (VIEIRA et al., 2004VIEIRA, S.; DE CAMARGO, P.B.; SELHORST, D.; DA SILVA,R.; HUTYRA, L.; CHAMBERS, J.Q.; BROWN, I.F.; HIGUCHI, N.; DOS SANTOS, J.; WOFSY, S.C.; TRUMBORE, S.E.; MARTINELLI, L.A. Forest structure and carbon dynamics in Amazonian tropical rain forest. Oecologia , v. 140, n. 3, p. 468-479, 2004.; CHAVE et al., 2005CHAVE, J.; ANDALO, C.; BROWN, S.; CAIRNS, M.; CHAMBERS, J.C.; EAMUS, D.; FÖLSTER, H.; FROMARD, F.; HIGUCHI, N.; KIRA, T.; LESCURE, J.; NELSON, B.W.; OGAWA, H.; PUIG, H.; RIÉRA, B.; YAMAKURA, T. Tree allometry and improved estimation of carbon stocks and balance in tropical forests. Oecologia, v.145, n.1, p.87-99, 2005.; MALHI et al., 2006MALHI, Y.; WOOD, D.; BAKER, T.R.; WRIGHT, J.; PHILLIPS, O.L.; COCHRANE, T.; MEIR, P.; CHAVE, J.; ALMEIDA, S.; ARROYO, L.; HIGUCHI, N.; KILLEEN, T.J.; LAURANCE, S.G.; LAURANCE, W.F.; LEWIS, S.L.; MONTEAGUDO, A.; NEILL, D.A.; NUNEZ-VARGAS, P.; PITMAN, N.C.A.; QUESADA, C.A.; SALOMÃO, R.; SILVA, J.N.M.; LEZAMA, A.T.; TERBORGH, J.; VÁSQUEZ MARTINEZ, R. The regional variation of aboveground live biomass in old-growth Amazonian forests. Global Change Biology, v.12, n. 7, p.1107-1138, 2006.; VIEIRA et al., 2008). The general trends for forests from high altitudes are the decline in stature and reduction in the aboveground biomass, while there is an increase in wood density (Aiba and Kitayama, 1999AIBA, S.; KITAYAMA, K. Structure, composition and species diversity in an altitude-substrate matrix of rain forest tree communities on Mount Kinabalu, Borneo. Plant Ecology, v.140, n. 2, p.139-157, 1999.; Moser et al., 2007MOSER, G.; HERTEL, D.; LEUSCHNER, C. Altitudinal change in LAI and stand leaf biomass in tropical montane forests: a transect study in Ecuador and a pantropical meta-analysis. Ecosystems, v.10, n. 6, p.924-935, 2007.). This pattern is a result of the limiting factors acting in these forests, mainly affecting photosynthesis, transpiration and nutrient availability (AIBA; KITAYMA, 1999AIBA, S.; KITAYAMA, K. Structure, composition and species diversity in an altitude-substrate matrix of rain forest tree communities on Mount Kinabalu, Borneo. Plant Ecology, v.140, n. 2, p.139-157, 1999.; RAICH et al., 2006RAICH, J.W.; RUSSELL, A.E.; KITAYAMA, K.; PARTON, W.J.; VITOUSEK, P.M. Temperature influences carbon accumulation in moist tropical forests. Ecology , v.87, n1., p.76-87, 2006.). However, Alves et al. (2010ALVES, L.F.; VIEIRA, S.A.; SCARANELLO, M.A.; CAMARGO, P.B.; SANTOS, F.A.M.; JOLY, C.A.; MARTINELLI, L.A. Forest structure and live aboveground biomass variation along an elevational gradient of tropical moist forest (Brazil). Forest Ecology and Management, v. 260, n.5, p.679-691, 2010.) found that in the Atlantic Forest, the biomass and abundance of large individuals are incremented with the increasing altitude.

Individuals with DBH ≥ 40 cm, even if weakly represented in the sampled area (1.6%) had influenced in the total biomass calculation - 43 Mg.ha-1 or 26% of that value. In contrast, the diameters inferior to 10 cm (48.7%) had accumulated only 6.7% or 11.1 Mg.ha-1of the total biomass (Figure 5). Considering the height, those higher than 20 m (1.7% of total) had 20% of the biomass (33.8 Mg.ha-1) and those with wood density equal or higher than 0.8 g.cm3 (11%) had 10.8% of the total biomass (18.02 Mg.ha-1). Medeiros and Aidar (2011MEDEIROS, M.C.M.P.; AIDAR, M.P.M. Structural variation and content of aboveground living biomass in an area of Atlantic Forest in the State of São Paulo, Brazil. Hoehnea, v.38, n.3, p. 413-428, 2011.) researching a plot at Montane Ombrophilous Dense Forest found that diameters of up to 13 cm comprised 60% of the individuals and 7.4% of the total biomass, similarly to the results found by Vieira et al. (2004VIEIRA, S.; DE CAMARGO, P.B.; SELHORST, D.; DA SILVA,R.; HUTYRA, L.; CHAMBERS, J.Q.; BROWN, I.F.; HIGUCHI, N.; DOS SANTOS, J.; WOFSY, S.C.; TRUMBORE, S.E.; MARTINELLI, L.A. Forest structure and carbon dynamics in Amazonian tropical rain forest. Oecologia , v. 140, n. 3, p. 468-479, 2004.) in a Central Amazon forest, where trees with diameters between 10 and 29.9 cm corresponded to approximately 80% of the individuals sampled, and contributed only with 26.4 to 32.9% of the total estimated biomass.

FIGURE 5
Distribution of aboveground biomass in the respective diameter classes at Santa Virgínia Nucleus. The y-axis represents live aboveground biomass (Mg.ha-1).

CONCLUSIONS

The forest studied in a secondary stage of regeneration, after significant past impact more than 40 years ago. However, if we consider the little amount of pioneers species (and individuals) and the higher number of early and late secondary species (and individuals) we can conclude that the site is evolving to a more mature condition along succession and could be considered in middle stage. We can predict that aboveground biomass accumulation would increase in the future decades, especially due to the change in the composition (TABARELLI; MANTOVANI, 1999TABARELLI, M.; MANTOVANI, W. A regeneração de uma Floresta Tropical Montana após corte e queima (São Paulo-Brasil). Brazilian Journal of Botany , v.59, n.2, p.239-250, 1999.). The results will help a better understanding of the gas exchanges between atmosphere and biosphere in the area and will provide subsidies for the development a model of carbon balance in the Montane Ombrophilous Dense Atlantic Forest from southeastern Brazil.

ACKNOWLEDGMENTS

The authors would like to thank people involved in fieldwork - Renato Belinello, Wagner Toledo, Mc. Fernanda Cassemiro, Ms. Filipe Pikart, Ms. Janaína Silva and Mc. Giampiero Bini Cano; plant identification - Dr. Maíra Padgurschi and staff of Vegetal Taxonomy Laboratory of Unicamp; and English review - Espaço da Escrita - Unicamp. This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), FAPESP Thematic projects “Carbon Tracker and Water Availability: Controls of Land Use and Climate Changes” (FAPESP 08/58120-3), and “Gradiente Funcional: Composição florística, estrutura e funcionamento da Floresta Ombrófila Densa dos Núcleos Picinguaba e Santa Virgínia, do Parque Estadual da Serra do Mar, São Paulo, Brasil” (Processo FAPESP 03/12595-7).

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Publication Dates

  • Publication in this collection
    Oct-Dec 2016

History

  • Received
    04 Oct 2016
  • Accepted
    25 Nov 2016
UFLA - Universidade Federal de Lavras Universidade Federal de Lavras - Departamento de Ciências Florestais - Cx. P. 3037, 37200-000 Lavras - MG Brasil, Tel.: (55 35) 3829-1706, Fax: (55 35) 3829-1411 - Lavras - MG - Brazil
E-mail: cerne@dcf.ufla.br