1 Universidade Federal de São Carlos, Núcleo de Estudos em Áreas Protegidas e Sustentabilidade, Sorocaba, SP, Brazil 2 Universidade Estadual Paulista, Programa de Pós Graduação em Ciências Florestais, Botucatu, SP, Brazil 3 Serviço de Apoio às Micro e Pequenas Empresas, Escritório Regional do Vale do Ribeira, Registro, SP, Brazil 4 Universidade Federal de São Carlos, Programa de Pós Graduação em Diversidade Biológica e Conservação, Sorocaba, SP, Brazil 5 Universidade Federal de São Carlos, Programa de Pós Graduação em Sustentabilidade na Gestão Ambiental, Sorocaba, SP, Brazil 6 Author for correspondence: cardosoleite@yahoo.com.br Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil ABSTRACT To study forest composition and structure, as well as to facilitate management plans and monitoring programs, we conducted a phytosociological survey in the PE Caverna do Diabo State Park and the Quilombos do Médio Ribeira Environmentally Protected Area, both located within the state of São Paulo, Brazil. We analyzed 20 plots of 400 m2 each, including only individuals with a circumference at breast height ≥ 15 cm. We employed cluster analysis and ordination (principal component analysis and correspondence analysis), including species data and abiotic data. We evaluated 1051 individuals, belonging to 155 species in 48 families. Of those 155, 18 were threatened species, 33 were endemic species, and 92 (59.4%) were secondary species. Th e overall Shannon index was 4.524, one of the highest recorded for a dense rainforest in southeastern Brazil. We found that our sample plots fell into three blocks. Th e fi rst was forest in which there had been human disturbance, showing low species richness, minimal density, and a small relative quantity of biomass. Th e second was undisturbed mature forest, showing a comparatively larger quantity of biomass. Th e third was mature forest in which there had been natural intermediate disturbance (dead trees), showing higher species richness and greater density. We identifi ed various groups of species that could be used in monitoring these distinct forest conditions. Key words: Biodiversity, intermediate disturbance, Atlantic Forest, forest monitoring Eliana Cardoso-Leite1,4,5, Diego Sotto Podadera2, Juliana Cristina Peres3 and Ana Carolina Devides Castello4 Submitted: 26 July, 2012. Accepted: 19 November, 2012 Acta Botanica Brasilica 27(1): 180-194. 2013. Introduction Although the Atlantic Forest biome originally covered roughly 150 million ha of Brazilian territory, only 11.73% remain. Th e largest fragments of dense rain forest are lo- cated in the Serra do Mar area, distributed throughout the states of Rio de Janeiro, São Paulo and Paraná (Ribeiro et al. 2009). Th e Atlantic Forest biome comprises the dense rain forest and related ecosystems—including open rain forest, Araucaria forest, mangrove, restinga (coastal woodland) and sand dune vegetation—and has garnered international at- tention because of its strategic importance, being one of the eight so-called “biodiversity hotspots” (Myers et al. 2000), as well as because of its high level of species endemism (Mittermeier 2005) and large number of endangered spe- cies (Brasil 2008). Th e dense rain forest is one of the world’s most threatened ecosystems. To preserve the diversity of biomes worldwide, there are specially protected areas (Dudley 2008), known in Brazil as conservation units (Brasil 2000). Th e state of São Paulo has 9000 ha of protected areas, approximately 40% of which are in the Vale do Ribeira, the location of our study sites. Studies on biodiversity can eff ectively promote conserva- tion of these areas, because knowledge of protected species is a prerequisite for effi cient management. Such studies can facilitate the development of management plans for these conservation units, as well as of monitoring programs for the ecosystems and species involved. Several studies have been conducted in order to profi le the biodiversity and ecological processes in protected areas of the Atlantic Forest biome in the various states within the southeastern region of Brazil, such as the works of Oliveira et al. (2001) and Mamede et al. (2004) at Juréia-Itatins Ecological Station (São Paulo); Kurtz & Araújo (2000) at Acta bot. bras. 27(1): 196-210. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 181 Paraíso State Ecological Station (Rio de Janeiro); Moreno et al. (2003) at Desengano State Park (Rio de Janeiro); Sztut- man & Rodrigues (2004) at Campina do Encantado State Park (São Paulo); Peixoto et al. (2004) at Serra da Capoeira Grande Environmentally Protected Area (Rio de Janeiro); Aidar et al. (2001), Guilherme et al. (2004) and Zipparro et al. (2005) at Alto Ribeira Touristic State Park (São Paulo); Guedes-Bruni et al. (2006) at Poço das Antas Biological Reserve (Rio de Janeiro); Catharino et al. (2006) at Morro Grande Forest Reserve (São Paulo); and Assis et al. (2011) and Rochelle et al. (2011) at Serra do Mar State Park – Pi- cinguaba base (São Paulo). All of those studies registered high woody species richness and a high Shannon diversity index (H’ = 2.88-4.75), demonstrating the importance of the conservation units (Brasil, 2000) in protecting the plant species of the Atlantic Forest biome. Th e study sites are located within the Jacupiranga Com- plex of conservation units (Estado de São Paulo 2008b). Th is Complex resulted from the redefi nition of the boundaries of the former Jacupiranga State Park and now comprises fourteen conservation units, with a total of 243,855.78 ha: three state parks, four environmentally protected areas, fi ve sustainable development reserves and two extractive reserves. Th ere have been no systematic surveys of woody species diversity in the conservation units within the Jacupiranga Complex. However, the protected areas of Brazil, including our study sites, have been suff ering the same problems seen in other countries, such as ecosystem degradation, encroachment and invalidation of the legal instrument of their creation (Terborg 2002). To avoid these problems and guarantee conservation eff ectiveness, the Brazilian National System of Conservation Units (Brasil 2000) requires that each conservation unit create its management plan within the fi rst fi ve years aft er its creation. Th e management plans are important instruments of planning and administration that direct management actions, establish research prio- rities, set forth restrictions and lay down guidelines for direct and indirect use of protected areas. Even though the importance of having a management plan is recognized by managers and government offi cials, those plans have yet to be devised for the Jacupiranga Complex, which was created in 2008. Th e aim of this study was to investigate woody species ri- chness and structure in the Jacupiranga Complex, especially within the Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area; analyzing the maturity of the plant community and discussing the conservation status of this forest, thereby facilitating the development of management plans for those two preserves. An additional objective was to collect preliminary data for the monitoring of terrestrial ecosystems in these protected areas, under the assumption that there are diff erences among the fragments of dense rain forest in the studied areas, and that these diff erences are related to physical features of the environment, as well as to natural or human disturbances. Material and methods Study site Th is study was conducted in the Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area, both part of the Jacupiranga Complex (Es- tado de São Paulo 2008), formerly known as Jacupiranga State Park (Lino 2009). Th e Caverna do Diabo State Park comprises 40,219.66 ha and the Quilombos do Médio Ri- beira Environmentally Protected Area comprises 64,625.04 ha. Th ese two preserves encompass an area stretching from 24°20’S to 24°46’S and from 48°03’W to 48°40’W and are distributed throughout the region in which the cities of Barra do Turvo, Cajati, Eldorado and Iporanga are located. Th e Jacupiranga Complex is located within the so-called “crystalline complex”, which has various lithologies, inclu- ding the Turvo-Cajati formation, the Costeiro granite belt, the Setuvas assemblage, the (Neoproterozoic) Açungui group, and post-tectonic granites (Almeida et al. 1981). Th e landscape is one of rolling hills (Ponçano et al. 1981). Th e vegetation is comprised of dense rain forest of various subtypes according to the altitude (Veloso et al. 1991; Brasil 1992): submontane, montane and high montane. Data collection We conducted a phytosociological survey in a dense rain forest (Fig. 1), using the plot method (Mueller Dumbois & Ellemberg 1974). We placed 20 plots of 400 m2 each (Fig. 1) in the proxi- mities of the following trails: Caverna (plots 1 and 2); Araçá (plots 3 to 11); and Bugio (plots 12 to 20). Th e Caverna trail grants access from the visitor center to the Diabo Cave and is approximately 150 m long. Th is trail further divides into two new trails, Araçá to the right, and Bugio to the left (Fig. 1). We placed 9 plots along each of the main trails (Araçá and Bugio), because they circle a group of hills that vary in orientation of sun exposure. On the Araçá trail, declivity, rockiness and the amount of incident light on soil are visibly greater, and the predominant exposure is east by northeast. On the Bugio trail, declivity, rockiness and the amount of incident light on soil are visibly lesser, and the predominant exposure is west by southwest. We placed only two plots on the Caverna trail, because of its short length. We sampled all woody individuals with a circumference at breast height ≥ 15 cm, collected botanical material for identifi cation and registered their height and circumference at breast height. Data were collected from 2005 to 2009. In all plots, we analyzed the physical features of the envi- ronment (abiotic factors), such as: rockiness, declivity, litter, human disturbance, canopy cover, and altitude. Rockiness was categorized on a four-point scale: 0 = no exposed rock within the plot; 1 = exposed rock in ≤ 10% of the plot; 2 = exposed rock in 11-30% of the plot; and 3 = exposed rock in > 30% of the plot. Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 182 Human disturbance was quantifi ed by assessing the following indicators: the presence of trash/garbage; evi- dence of fi re; felled trees; and evidence of domesticated animals. Human disturbance was categorized as follows: 0 = no impact; 1 = positive for one indicator to a low degree; 2 = positive for two or more indicators to a low degree; and 3 = positive for two or more indicators to a moderate degree or for one indicator to a high degree. Litter was also categorized on a four-point scale, based on the depth of the litter layer: 0 = completely decomposed; 1 = 1-3 cm; 2 = 3-6 cm; and 3 = > 6 cm. To obtain the litter layer thickness values, we randomly measured 10 points within the plot and calculated the mean. Declivity was categorized as follows: 0 = fl at or gently sloping terrain (0-10°); 1 = moderately steep terrain (11- 20°); 2 = steep terrain (21-44°); 3 = very steep terrain (≥ 45°). Altitude was measured directly with an altimeter. To quantify canopy cover, we used a densiometer and calculated the percentage of canopy cover. Data analysis We identifi ed all species with the use of dichotomous keys and literature on the taxa; through comparison with specimens on fi le at recognized herbaria (those of the University of São Paulo Luiz de Queiroz Graduate School of Agriculture, the São Paulo State University at Campinas and the São Paulo State Botanical Institute); and with the aid of specialists. Species identifi cation followed the An- giosperm Phylogeny Group II guidelines (APG II 2003; Souza & Lorenzi 2005). Voucher specimens were deposited at the Herbarium of the Federal University of São Carlos at Sorocaba Center for Sustainability Science and Technology. We defi ned endangered species as those listed as such on the São Paulo State List of Endangered Plant Species (Estado de São Paulo 2008a), the Brazilian National List of Endangered Plant Species (Brasil 2008) and the International Union for Conservation of Nature Red List of Th reatened Species (IUCN 2012). We defi ned species endemic to the Atlantic Forest biome were defi ned as those having a geographic distribution restricted to the biome and cited as being endemic to Brazil in the 2012 List of Species in the Flora of Brazil (Forzza et al. 2012). Th e species identifi ed were compared with other studies of this nature through SSI = Sorensen similarity index. All species were categorized in ecological or successio- nal groups according to Budowski (1965): pioneer, early secondary, late secondary and climax. Species classifi cation was based on our own fi eld experience, direct observation and data from the literature, especially the studies of Leitão Filho (1993) and Gandolfi (1995). Species without enough references were deemed “uncategorized”. According to Catharino et al. (2005), a correct classifi cation of species into functional groups depends upon the knowledge of the species biology and the adaptation of data from classic authors (Budowsky 1965; Denslow 1980; Whitmore 1989). To avoid classifi cation errors and facilitate data analysis, the four groups were united into two—pioneer sensu lato Figure 1. A- Map of the Jacupiranga Complex. B- Aerial image of the Jacupiranga Complex (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W) and of the plots sampled in the present study. *Th e quilombolas are members of the quilombos, communities established by freed slaves. Source (A): Instituto Socioambiental, 2008. Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 183 (pioneer and early secondary) and non-pioneer sensu lato (late secondary and climax)—in agreement with the clas- sifi cation system devised by Whitmore (1989). To identify the development stage of the forest, we analyzed the relative proportion of pioneer and non-pioneer species and indi- viduals, considering a value above 50% as an indicator of a certain successional stage, a procedure also adopted by Dislich et al. (2001). We analyzed the following phytosociological parame- ters: absolute and relative density; absolute and relative do- minance; cover value; and Shannon diversity index (H’). We conducted a cluster analysis with the unweighted pair group method with arithmetic mean and Bray-Curtis similarity, using a matrix of sampling units and total species number. We also conducted a principal components analysis (PCA), using a matrix of sampling units and number of individuals per species (selecting species with 10 or more individuals). Using this same matrix and adding the data of abiotic factors for each plot, we conducted a correspon- dence analysis (CA). In this case, the altitude and canopy cover data were grouped in four classes to improve graph visualization. All phytosociological analyses were conducted with the soft ware Fitopac 2.1 (Shepherd 2009). Th e cluster analysis indicated three distinct clusters of sampling units, and a similar result was obtained in the CA (the analyses were conducted with the total number of plots, regardless of their location in fi eld). Th e groups of plots obtained in the CA were compared with Student’s t-test (Zar 1996) in terms of phytosociological parameters number of species, total density and biomass (volume and basal area), with the soft ware BioEstat 5.0 (Ayres et al. 2007). Th ese groups of plots were also tested in terms of number of dead trees and number of individuals of Euterpe edulis (t-test with 5% signifi cance level), due to the large number of dead trees and the small number of individuals of E. edulis within the study site. Because the occurrence of E. edulis was greater in the group of plots with the largest number of dead trees, highest density of individuals and greatest species richness, we con- ducted Pearson’s correlation tests between the number of dead trees and number of E. edulis individuals; between total density and number of E. edulis individuals; and between species richness and number of E. edulis individuals. All of those tests were conducted with the soft ware BioEstat 5.0 (Ayres et al. 2007). Results and discussion We sampled 1501 individuals belonging to 155 species in 48 families (Tab. 1). Density was 1313.75 ind./ha, and the basal area was 36.45 m2/ha. Th e Shannon diversity index was 4.524, with an evenness of 0.897. Myrtaceae, Fabaceae (or Leguminosae), Rubiaceae, Meliaceae and Lauraceae were the families with the highest richness and, together with 15 other families (Fig. 2), accounted for 75.36% of the total species and 91.15% of the total individuals. Fabaceae was the family with the greatest number of individuals, follo- wed by Myrtaceae and Rubiaceae. Th e genera with highest species richness were: Eugenia (9), Myrcia (7), Maytenus (4), Machaerium (4), Nectandra (4), Miconia (4), Trichilia (4) and Zanthoxylum (4). No exotic species were sampled within the plots. Our results are in agreement with those of other studies of the Atlantic Forest in southeastern and southern Brazil, in which Myrtaceae and Fabaceae were found to be the families with highest species richness. Rochelle et al. (2011) conducted a review of 28 such studies and found that species richness was highest for Myrtaceae in 21 of those studies, whereas it was highest for Fabaceae in four. Most studies conducted in dense rain forest in the state of São Paulo (Melo & Mantovani 1994; Melo et al. 2000; Guilherme, 2004; Zi- pparro et al. 2005; Catharino et al. 2006) show Myrtaceae as the richest family, usually followed by Fabaceae, Rubiaceae, Lauraceae, Melastomataceae and Euphorbiaceae. Many of the species endemic to the Atlantic Forest (Tab. 1) belong to Myrtaceae. In studies conducted in dense rain forest, the genus Eugenia is cited as having the largest number of species (Rochelle et al. 2011; Scudeller et al. 2001). Oliveira Filho & Fontes (2000) asserted that, in such forests, Myrta- ceae is the richest family, the richest genera being Eugenia, Myrcia, Miconia and Ocotea. In the present study, the species with the highest cover values included the pioneers Anadenanthera colubrina, Piptadenia gonoacantha, Alchornea triplinervia, and Senna multijuga, as well as the non-pioneers Ficus enormis, Cryp- tocarya aschersoniana, Casearia obliqua, Campomanesia guaviroba, Myrcia splendens, Cabralea canjerana, Bathysa australis, Chrysophyllum marginatum, Eugenia mosenii, Guapira opposita, and Chrysophyllum sp. (Tab. 1), collecti- vely accounting for 41.3% of the total cover value (Fig. 3). In a study conducted near the municipality of Ubatuba, in the state of São Paulo, Ramos et al. (2011) reported that B. australis and G. opposita were the species with the largest cover values, whereas Guilherme et al. (2004) reported that B. australis, G. opposita and A. triplinervia were among the species with largest cover value at Intervales State Park, also within the state of São Paulo. In the present study, despite having a relatively large number of individuals (n = 22), E. edulis ranked 30th in cover value, because all of those individuals were small in diameter. Th is contrasts with the results of most studies conducted in dense rain forests, in which E. edulis occupied the fi rst positions either in cover value or importance value (Mamede et al. 2004; Ramos et al. 2011; Guilherme et al. 2004). Th is fi nding raises concern, because E. edulis is an endangered species in Brazil and in the state of São Paulo. Th erefore, one would expect that, especially within an area of total conservation, it would be protected. Dead individuals (treated as a single species) occupied the fi rst position in cover value, emphasizing the intense Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 184 Continues Table 1. Species sampled within the Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). Species Individuals Collector Abbreviation Ecological group Endangered status Exclusive to the AF of Brazil Cover valuen I.D. Geographic range-threat level Dead individuals 84 - 13.42 Anadenanthera colubrina (Vell.) Brenan 19 1233 A col P No 7.44 Ficus enormis (Miq.) Miq. 10 237 F eno NP No 7.02 Piptadenia gonoacantha (Mart.) J.F.Macbr. 17 703 P gono P No 6.50 Alchornea triplinervia (Spreng.) Müll.Arg 15 655 A tri P No 6.13 Cryptocarya aschersoniana Mez 9 83 C asch NP No 4.89 Casearia obliqua Spreng. 35 190 C obli NP No 4.63 Senna multijuga (Rich.) H.S. Irwin & Barneby 19 289 S mult P No 4.12 Campomanesia guaviroba (DC.) Kiaersk. 22 760 C gua NP No 4.11 Myrcia splendens (Sw.) DC. 9 1236 M spl NP No 4.03 Cabralea canjerana (Vell.) Mart. 21 335 C canj NP No 3.97 Bathysa australis (A. St.-Hil.) Hook. f. ex K. Schum. 22 1499 B aus NP No 3.93 Chrysophyllum marginatum (Hook. & Arn.) Radlk 20 384 C marg NP SP-NT No 3.51 Eugenia mosenii (Kausel) Sobral. 16 05 E mos NP Yes 3.20 Guapira opposita (Vell.) Reitz 29 1430 G opp NP No 3.09 Chrysophyllum sp. 5 346 C sp NP No 3.00 Machaerium stipitatum (DC.) Vogel 4 249 M sti P No 2.86 Hieronyma alchorneoides Allemão 9 1477 H alc P No 2.81 Virola bicuhyba (Schott ex Spreng.) Warb. 6 1467 V bic NP Yes 2.76 Annona dolabripetala Raddi 12 671 A dol NP Yes 2.64 Myrcia defl exa (Poir.) DC. 11 408 M defl NP No 2.50 Prockia crucis L. 20 117 P cru P No 2.45 Machaerium sp.1 12 216 M sp - No 2.45 Dahlstedtia pinnata (Benth.) Malme 21 323 D pin NP Yes 2.44 Coussarea contracta var. contracta 17 371 C contr NP No 2.41 Indet 1 2 In1 - No 2.37 Pera glabrata (Schott) Poepp. ex Baill. 15 743 P gla P No 2.35 Guatteria nigrescens Mart. 18 1333 G nig NP No 2.26 Nectandra grandifl ora Nees & C. Mart. ex Nees 11 247 N gran NP No 2.24 Euterpe edulis Mart. 22 860 E edu NP BR-EN; SP-VU No 2.23 Tibouchina mutabilis (Vell.) Cogn. 9 1145 T mut P Yes 2.09 Mollinedia uleana Perkins 17 1260 M ule NP Yes 1.99 Pisonia ambigua Heimerl 11 86 P amb NP No 1.99 Coussarea contracta var. panicularis Müll.Arg. 9 35 C cont NP No 1.99 Sloanea monosperma Vell. 9 1221 S mon NP No 1.96 Casearia sylvestris Sw. 12 1234 C syl P No 1.92 Allophylus edulis (A. St.-Hil., A. Juss. & Cambess.) Hieron. ex Niederl. 17 953 A edu P No 1.90 Eugenia cuprea (O. Berg) Mattos 9 112 E cup NP Yes 1.82 Gomidesia spectabilis (DC.) O. Berg (sin. Myrcia spectabilis DC.) 14 02 G spec NP Yes 1.74 Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 185 Species Individuals Collector Abbreviation Ecological group Endangered status Exclusive to the AF of Brazil Cover valuen I.D. Geographic range-threat level Mollinedia schottiana (Spreng.) Perkins 12 354 M sch NP Yes 1.70 Rudgea jasminoides (Cham.) Müll.Arg. 14 209 R jasm NP No 1.61 Cinnamomum glaziovii (Mez) Kosterm. 2 680 C gla NP Yes 1.60 Cupania oblongifolia Mart. 11 715 C oblo NP No 1.57 Schizolobium parahyba (Vell.) S.F.Blake 5 917 S par P No 1.57 Clusia criuva Cambess. 10 777 C cri P Yes 1.57 Psychotria suterella Müll.Arg. 15 822 P sut NP No 1.55 Nectandra megapotamica Spreng. Mez 9 870 N meg NP No 1.52 Myrocarpus frondosus Allemao 4 734 M fron NP WW-DD, SP-NT No 1.44 Garcinia gardneriana (Planch. & Triana) Zappi 9 308 G gar NP No 1.43 Machaerium scleroxylon Tul. 12 751 M scle NP No 1.30 Eugenia aff stictosepala Kiaersk. 10 280 E stic NP No 1.29 Syagrus romanzoffi ana (Cham.) Glassman 5 1238 S rom NP No 1.17 Cedrela fi ssilis Vell. 5 659 C fi ss NP WW-EN, SP-NT No 1.15 Prunus sellowii Koehne 2 1150 P sel P No 1.13 Indet 2 2 In2 - No 1.10 Eugenia blastantha (O.Berg) D.Legrand 4 43 E bla NP No 0.93 Hedyosmum tepuiense Todzia (sin. Hedyosmum brasiliense Miq.) 1 1163 H tep NP No 0.99 Cryptocarya moschata Nees & Mart. 7 718 C mos NP No 0.92 Inga marginata Willd. 8 956 I mar P No 0.91 Guarea kunthiana A. Juss. 4 353 G kun NP SP-NT No 0.90 Maytenus alaternoides Reissek 8 359 M ala NP No 0.90 Machaerium aculeatum Raddi 6 271 M acu P No 0.87 Eugenia monosperma Vell. 4 1182 E mon NP Yes 0.87 Nectandra leucantha Nees & Mart. 4 811 N leu NP SP-NT Yes 0.85 Sapium glandulosum (L.) Morong 7 761 S gla P No 0.84 Solanum aff caavurana Vell. 6 808 S caa P No 0.84 Cestrum axillare Vell. 7 709 C axi P No 0.84 Campomanesia neriifl ora (O.Berg.) Nied. 5 1255 C ner NP WW-VU Yes 0.79 Alseis fl oribunda Schott 5 1470 A fl o NP No 0.79 Xylopia brasiliensis Spreng. 5 142 X bra NP Yes 0.78 Eugenia brasiliensis Lam. 3 179 E bra NP No 0.78 Cecropia glaziovii Snethl. 5 1404 C gla P Yes 0.77 Citronella megaphylla (Miers) R.A. Howard 7 231 C meg P No 0.76 Guarea sp. 6 278 G sp - No 0.76 Coutarea hexandra (Jacq.) K. Schum. 6 894 C hex NP No 0.74 Lonchocarpus muehlbergianus Hassl. 3 1210 L mue NP No 0.72 Sorocea bonplandii (Baill.) W.C.Burger, Lanj. & de Boer 2 397 S bon NP No 0.71 Pseudobombax grandifl orum (Cav.) A. Robyns 3 1453 P gra P No 0.67 Cordia aff sellowiana Cham 3 319 C sel P No 0.64 Table 1. Continuation. Continues Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 186 Species Individuals Collector Abbreviation Ecological group Endangered status Exclusive to the AF of Brazil Cover valuen I.D. Geographic range-threat level Quiina glaziovii Engl. 4 21 Q gla NP No 0.63 Zanthoxylum riedelianum Engl. 6 802 Z rie P No 0.63 Sessea brasiliensis Toledo 4 98 S bra NP WW-DD Yes 0.62 Miconia cinnamomifolia (DC.) Naudin 5 1190 M cin NP Yes 0.56 Nectandra oppositifolia Nees & Mart. 3 754 N opp P No 0.54 Parinari excelsa Sabine 3 390 P exc NP No 0.53 Myrcia sp2 4 897 M sp2 - No 0.52 Psychotria mapourioides DC. 4 700 P map NP No 0.52 Pouteria caimito (Ruiz & Pav.) Radlk. 4 97 P cai NP No 0.51 Dalbergia frutescens (Vell.) Britton 3 904 D fru NP No 0.50 Meliosma sellowii Urb. 4 137 M sel P No 0.49 Miconia cf brachybotrya Triana 3 08 M bra P No 0.49 Coussapoa microcarpa (Schott) Rizzini 1 90 C mic P No 0.49 Aspidosperma ramifl orum Müll.Arg. 2 1183 A ram NP No 0.48 Bunchosia maritima (Vell.) J.F. Macbr. (sin. B. fl uminensis Griseb) 4 706 B mar NP No 0.48 Cariniana legalis (Mart.) Kuntze 1 1162 C leg NP WW-VU, SP-NT No 0.48 Strychnos sp. 4 1458 S sp - No 0.45 Guarea macrophylla subsp. macrophylla 4 838 G mac NP SP-NT No 0.44 Weinmannia paulliniifolia Pohl 1 674 W pau P Yes 0.44 Marlierea suaveolens Cambess. 4 99 M sua NP SP-VU Yes 0.43 Posoqueria latifolia (Rudge) Roem. & Schult. 3 422 P lat NP No 0.43 Annona sylvatica A. St.-Hil ( sin - Rollinia sylvatica (A. St.-Hil.) Martius) 4 806 A syl P Yes 0.42 Miconia cabussu Hoehne 4 1155 M cab NP Yes 0.41 Solanum argenteum Dunal 3 1192 S arg P No 0.38 Trichilia claussenii C. DC. 3 717 T cla NP No 0.38 Lonchocarpus guillemineanus (Tul.) Malme 3 1172 L gui P No 0.37 Coccoloba sp. 2 1143 Co sp - No 0.36 Terminalia trifl ora (Griseb) Lillo 2 1219 T tri - No 0.35 Zanthoxylum rhoifolium Lam. 3 668 Z rho P No 0.34 Solanaceae sp. 3 1454 Sol - No 0.34 Ficus obtusifolia Kunth 3 156 F obt - No 0.32 Clethra scabra Pers. 3 739 C sca P No 0.32 Myrcia sosias D.Legrand 3 660 M sos NP No 0.31 Croton sp. 2 1418 Cr sp - No 0.31 Esenbeckia febrifuga (A. St.-Hil.) A. Juss. ex Mart. 1 09 E feb NP No 0.31 Trichilia pallens C. DC. 2 569 T pal NP WW-NT No 0.30 Platymiscium fl oribundum Vogel 2 92 P fl or NP No 0.30 Malouetia cestroides (Ness) Mull. Arg. 2 1140 M ces P Yes 0.29 Luehea sp. 1 815 Lu sp - No 0.29 Myrsine coriacea (Sw.) R. Br. ex Roem. & Schult. 2 764 M cor P No 0.29 Table 1. Continuation. Continues Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 187 Species Individuals Collector Abbreviation Ecological group Endangered status Exclusive to the AF of Brazil Cover valuen I.D. Geographic range-threat level Tetrastylidium grandifolium (Baill.) Sleumer 1 365 T gran NP Yes 0.25 Celastraceae sp1 2 750 Cel - No 0.24 Myrsine guianensis (Aubl.) Kuntze 2 394 M gui P No 0.24 Myrceugenia myrcioides (Cambess.) O.Berg 2 213 M myr NP WW-NT Yes 0.24 Ilex theizans Mart. ex Reissek 1 826 I the NP No 0.23 Jacaratia spinosa (Aubl.) A.DC. 2 307 J spi P No 0.22 Eugenia subterminalis DC. (sin. E. psidiifl ora O. Berg., C. pisidiifl orus (O. Berg) Sobral) 2 344 E sub NP No 0.22 Rubiacaea sp.1 1 1283 Rub1 - No 0.22 Myrsinaceae sp 2 232 Myrs1 - No 0.22 Myrceugenia campestris (DC.) D.Legrand & Kausel 2 1433 M camp NP WW-VU No 0.21 Protium widgrenii Engl. 2 708 P wid NP No 0.21 Myrcia hatschbachii D. Legrand 2 752 M has NP Yes 0.21 Zanthoxylum petiolare A. St.-Hil. & Tul. 2 663 Z pet P SP-VU Yes 0.20 Maytenus offi cinalis Mabb (sin. Maytenus ilicifolia Mart. ex Reissek) 2 1200 M off NP SP-EX No 0.20 Actinostemon communis (Müll. Arg.) Pax 1 297 A com P No 0.18 Myrcia sp1 1 1472 M sp1 - No 0.13 Connarus regnellii G. Schellenb. 1 780 C reg NP Yes 0.13 Eugenia pruinosa D. Legrand 1 70 E pru NP Yes 0.12 Trichilia silvatica C. DC. 1 417 T sil NP WW-VU Yes 0.12 Cariniana estrellensis (Raddi) Kuntze 1 1162 C est NP SP-NT No 0.11 Pourouma sp. 1 277 Po sp - No 0.11 Ocotea laxa (Nees) Mez 1 1186 O lax NP Yes 0.11 Maytenus evonymoides Reissek 1 192 M evo NP No 0.11 Fabaceae sp.1 1 351 Fab1 - No 0.11 Chomelia brasiliana A. Rich. 1 62 C bra NP No 0.11 Marlierea racemosa (Vell.) Kiaersk. 1 1329 M rac NP No 0.11 Miconia sp. 1 224 Mi sp - Yes 0.11 Eugenia stigmatosa DC. 1 745 E sig NP Yes 0.10 Handroanthus serratifolius (Vahl) S. O. Grose 1 44 H serr NP No 0.10 Miconia centrodesma Naudin 1 1212 M cen P No 0.10 Apeiba tibourbou Aubl. 1 343 A tib P No 0.10 Piper cf gaudichaudianum Kunth 1 124 P gau NP No 0.10 Maytenus robusta Reissek 1 285 M rob NP No 0.10 Physalis sp. 1 263 Ph sp - No 0.10 Trichilia catigua A. Juss. 1 534 T cat NP No 0.10 Aspidosperma parvifolium A. DC. 1 87 A par NP No 0.10 AF – Atlantic Forest (biome); P – pioneer; NP – non-pioneer; SP – (state of) São Paulo (Estado de São Paulo 2004); BR – Brazil (Brasil 2008); WW – worldwide (IUCN 2012); EX – extinct; EN – endangered; VU – vulnerable; NT – near threatened; DD – data defi cient) Table 1. Continuation. Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 188 dynamics of this rain forest. In other studies, dead indivi- duals (when counted/reported) have usually ranked high, although not fi rst, in cover value, being second and sixth in the study conducted by Ramos et al. (2011), third in the study conducted by Rochelle et al. (2011) and second in the study conducted in a young forest by Aidar et al. (2001). Th e presence of dead individuals and of E. edulis individuals seems related, because both occurred mainly in the plots on the Araçá trail (plots 12-20), as will be discussed in detail. The comparison of our results with those of other studies in protected areas of diff erent subtypes of dense rain forest (Tab. 3) indicated greatest similarity with the Intervales State Park and Alto Ribeira Touristic State Park, followed by the Ilha do Cardoso State Park and Jureia-Itatins Ecological Station, all located within the Ribeira Valley. Figure 2. Families with highest richness of species and individuals (collectively accounting for 75.64% of the total species and 91.15% of the total individuals) in the Jacupiranga Complex – Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). Figure 3. Species with greatest cover value (accounting for 41.30% of the total cover value) in the Jacupiranga Complex – Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). Geographical distance apparently aff ected the similarity, because Intervales State Park, Ilha do Cardoso State Park and Jureia-Itatins Ecological Station are the areas closest to the Jacupiranga Complex (Tab. 3). Th e Intervales State Park and the Alto Ribeira Touristic State Park are located at altitudes similar to that of the Ribeira Valley, which might explain the occurrence of species in common. Th e lowest similarities were between our sites and coastal areas in the northern parts of the states of São Paulo and Rio de Janeiro, probably infl uenced by the greater geographical distance. Th e species diversity index in the present study was one of the greatest among the areas compared and was similar to that obtained by Rochelle et al. (2011) for the Serra do Mar State Park – Picinguaba base (Tab. 3). It was also higher than those recorded for the Juréia-Itatins Ecological Station and Intervales State Park, areas in which species richness is higher than at our site. Th is can be explained by the fact that the evenness was greater for our study site (0.897) than for those two preserves (0.818 and 0.75, respectively). Th erefore, species diversity in the Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area is high and similar to that of other montane and submontane dense rain forests in southeastern Brazil. We observed 18 threatened species (Tab. 1), of which 12 are listed as endangered in the state of São Paulo (Estado de São Paulo 2007), one (E. edulis) is listed as endangered in Brazil (Brasil 2008) and nine are listed as endangered worl- dwide (IUCN 2012). Most endangered species had a very small number of individuals. Th is indicates that even within protected areas these species are still at risk of extinction and underscores the importance of these areas, as well as the necessity of monitoring and thorough inspection to ensure the eff ective conservation of these populations. Few of the fl oristic and phytosociological surveys conducted in the states of São Paulo and Rio de Janeiro have identifi ed endan- gered species, except the works of Catharino et al. (2006), who reported 31 endangered species (11.9% of the species sampled) at Morro Grande Forest Reserve, and of Ramos et al. (2011), who reported 10 endangered species (5.18% of the species sampled) in the municipality of Ubatuba. Of the 157 species sampled in the present study, 33 are endemic to the Atlantic Forest (Tab. 1). Myrtaceae was the family with the largest number of endemic species. Analyzing the sets of endangered and endemic species (18 and 33, respectively), we observed seven species that belong to both groups, that is, species that occur in a restricted distribution and are endangered. Th ese species require special conser- vation eff orts to ensure maintenance of viable populations, which again underscores the importance of protected areas for the conservation of biodiversity in the Atlantic Forest. Th e classifi cation of species into ecological groups resulted in pioneer species accounting for 27.1%, non- -pioneer species accounting for 59.4% and uncategorized species accounting for 13.5% (Tab. 4). Of the total number of individuals, 25.9% were of pioneer species, 61.1% were Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 189 Table 2. Abiotic factors measured in sampling units, Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). Plot Rockiness Declivity Litter Human disturbance Cover Altitude Class Class Class Class % = class m = class 1 C 3 3 3 0 97.9 = 4 472 = 1 2 C 1 3 2 0 97.9 = 4 458 = 1 3 B 1 1 0 2 87.5 = 1 464 = 1 4 B 0 0 1 0 97.9 = 4 528 = 3 5 B 2 1 2 1 91.6 = 2 567 = 4 6 B 0 3 2 0 91.6 = 2 527 = 3 7 B 1 3 1 1 97.9 = 4 550 = 3 8 B 1 3 3 2 98.75 = 4 559 = 4 9 B 3 3 2 0 98.75 = 4 573 = 4 10 B 1 3 1 0 95.8 = 3 569 = 4 11 B 1 3 2 0 98.75 = 4 555 = 4 12 A 0 1 2 0 96.6 = 4 526 = 3 13 A 3 2 2 0 97.9 = 4 563 = 4 14 A 0 3 3 0 98.75 = 4 583 = 4 15 A 1 3 2 2 98.75 = 4 540 = 3 16 A 2 1 1 0 97.9 = 4 544 = 3 17 A 1 3 1 0 98.75 = 4 586 = 4 18 A 0 3 1 0 96.6 = 4 562 = 4 19 A 1 2 1 0 98.75 = 4 539 = 3 20 A 2 3 1 0 96.6 = 4 541 = 3 A – on the Araçá trail; B – on the Bugio trail; C – on the Caverna trail of non-pioneer species and 13% were of uncategorized species. Other studies in dense rain forest have reported that pioneers represent 44-62% of species in disturbed sites and 22-48% of species in preserved or mature sites. Th erefore, the proportion of pioneers in our study was relatively low. For non-pioneer species, the reported values range from 49% to 65% for preserved or mature areas. In the dense rain forest evaluated in our study, which can be considered mature or well preserved in comparison with other areas, 59.4% of the species were non-pioneers. Th e same result was obtained when we used the criterion of the dominant group (50% or more of species), because the ratio of non-pioneer to pioneer species was 2.19 and the ratio of non-pioneer to pioneer individuals was 2.36. Th e results of the cluster analysis of species data indica- ted three clusters of plots (fusion level 0.80), with a cophe- netic correlation of 0.832. Th e fi rst cluster (B) comprised plots 4-11 (all on the Bugio trail) and plot 12 (on the Araçá trail). Th e second cluster (A) comprised plots 13-20 (all on the Araçá trail), with two subclusters, the fi rst with plots 13, 14, 15, 16 and 19, and the other with plots 17, 18 and 20. Th e third cluster (C) comprised plots 1 and 2 (on the Caverna trail), together with plot 3 (on the Bugio trail). Th ese results demonstrate that, although the plots on the Araçá trail are diff erent from those on the Bugio trail, plot 12 (on the Araçá trail) is more similar to the cluster B plots and plot 3 (on the Bugio trail) is more similar to the cluster C plots. Th is might be related to the geographical distribution of the plots (Fig. 1), to the physical features of the environment or to diff erent levels of disturbance in these clusters. Th e fi rst two axes of the PCA explained 18.27% and 13.47% of total variation, respectively (Fig. 5). In the fi rst quadrant (positive for both axes), there was a cluster com- prising plots 13-16 (all on the Araçá trail), within which we identifi ed the species E. edulis, Guatteria nigrescens, Psychotria suterella, C. obliqua, Cupania oblongifolia, F. enormis, Clusia criuva, Machaerium scleroxylon and A. triplinervia, as well as dead individuals. In the second quadrant (negative for axis 1 and positive for axis 2), there was a cluster comprising plots 4-7 and 9-11 (all on the Bugio trail), together with plot 12 (on the Araçá trail). Within that cluster, we identi- fi ed the species Nectandra grandifl ora, Rudgea jasminoides, Coussarea contracta, G. opposita, Myrcia spectabilis, Myrcia defl exa, Mollinedia schottiana and Mollinedia uleana. Th is is agreement with the results of the cluster analysis, in which plot 12 was more similar to the cluster B of plots. In the third Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 190 Table 3. Comparison between this study (Jacupiranga Complex – Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area, from 24°20’S to 24°46’S and from 48°03’W to 48°40’W) and other studies in protected areas of dense rain forest in two states of southeastern Brazil. Study site Forest subtype Method, sample area Inclusion criterion Richness H’ SSI Reference n of species Juréia-Itatins Ecological Station - SP Submontane 10 plots, 10 × 20 m (0.2 ha) DBH ≥ 5 cm (Class IV) 63 3.38 0.156 Oliveira et al. (2001) Juréia-Itatins Ecological Station-SP Lowland 50 plots, 10 × 20 m (1 ha) DBH ≥ 5 cm 173 4.21 0.287 Mamede et al. (2004) Ilha do Cardoso State Park-SP Lowland, submontane 40 plots, 10 × 25 m (1 ha) CBH ≥ 8 cm 157 3.64 0.295 Melo & Mantovani (1994) Intervales State Park-SP Submontane 88 plots, 15 × 15 m (1.98 ha) DBH ≥ 5 cm 172 3.85 0.324 Guilherme et al. (2004) Alto Ribeira Touristic State Park- SP Montane Transect, 20 × 50 m (0.1 ha) CBH ≥ 15 cm 87 - 0.306 Aidar et al. (2001) Serra Mar State Park - SP Submontane 193 3.56- 4.05 0.236 Ramos et al. (2011) Serra Mar State Park-SP Submontane 100 plots, 10 × 10 m (1 ha) CBH ≥ 15 cm 206 4.48 0.216 Rochelle et al. 2011 Serra C.Grande Environmentally Protected Area-RJ Lowland Quadrant, 200 points CBH ≥ 15 cm 44 2.42 0.080 Peixoto et al. (2005) Paraíso Ecological Station- RJ Submontane Quadrant, 200 points DBH ≥ 5 cm 138 4.20 0.143 Kurtz & Araújo (2000) Desengano State Park-RJ Lowland, submontane 10 plots, 30 × 40 m (1.2 ha) DBH ≥ 10 cm 210 4.21- 4.30 0.132 Moreno et al. (2003) Morro Grande Forest Reserve-SP Montane Quadrant, 600 points DBH ≥ 5 cm 260 4.75 0.251 Catharino et al. (2006) Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area-SP Submontane 20 plots, 20 × 20 m (0.8 ha) CBH ≥ 15 cm 155 4.52 Current study SP – São Paulo; RJ – Rio de Janeiro; DBH – diameter at breast height; CBH – circumference at breast height; H’ – Shannon diversity index; E – evenness; SSI – Sørensen similarity index. quadrant (positive for axis 1 and negative for axis 2), there was a cluster comprising plot 1 (on the Caverna trail), plot 3 (on the Bugio trail), plot 18 and plot 19 (both on the Araçá trail). Within that cluster, we identifi ed the species P. gonoacantha, Allophylus edulis, S. multijuga, Machaerium aculeatum, A. co- lubrina, Casearia sylvestris, Annona dolabripetala, Dahlstedtia pinnata and Prockia crucis. Finally, in the fourth quadrant (negative for both axes), there was a cluster comprising only plot 2 (on the Caverna trail) and plot 20 (on the Araçá trail). Within that cluster, we identifi ed the species C. marginatum and Pisonia ambigua. Th e fi rst two axes of the CA explained 16.73% and 15.15% of the total variation, respectively (Fig. 6). Th e abiotic factors did not strongly infl uence the ordination of the plots, because most of those factors (rockiness, declivity, canopy cover and altitude) were located in the fi rst quadrant, close to zero. In this quadrant, there was also a cluster (Ba) composed of plots 4-11 (on the Bugio trail), together with plots 12, 18 and 20 (all on the Araçá trail). Within cluster Ba, we identifi ed the species C. contracta, R. jasminoides, M. deflexa, B. australis, M. spectabilis, G. opposita, M. uleana, P. ambigua, N. grandifl ora, A. dolabripetala and C. marginatum. In the third quadrant, there was a cluster (A) comprising plots 13-17 and 19 (all on the Araçá trail), un- related to the abiotic factors, within which we identifi ed the species E. edulis, C. obliqua, A. triplinervia, C. oblongifolia, Pera glabrata, G. nigrescens, A. edulis and M. scleroxylon, as well as dead individuals. In the fourth quadrant, there was a cluster with human disturbance (cluster Cb) comprising plots 1 and 2 (on the Caverna trail), as well as plot 3 (on the Bugio trail). Within cluster Cb, we identifi ed the species S. multijuga, P. crucis, A. colubrina, F. enormis, M. aculeatum, C. guaviroba and C. sylvestris, all of which, with the excep- tions of F. enormis and C. guaviroba, were pioneers. Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 191 Because the CA (Fig. 6) indicated three distinct clusters of sampling units (A, Ba and Cb), we compared the phyto- sociological parameters (number of species, total density, volume and basal area) of these clusters with a t-test. Total species richness was signifi cantly higher for cluster A, followed by clusters Ba and Cb, with means of 33.3, 29.7 and 18.3, respectively (p-values were 0.8536 for C vs. Ba; 0.8286 for Cb vs. A; and 0.2526 for Ba vs. A). In addition, the plots of cluster A had higher total density than did those of the clusters Ba and Cb, with mean densities of 1820 ind/ ha, 1136.6 ind/ha and 950 ind/ha, respectively (p-values were 0.8253 for A vs. Ba; 0.6485 for A vs. Cb; and 0.1844 for Ba vs. Cb). In contrast, the plots of cluster Ba had higher biomass (volume and basal area) than did those of clusters A and Cb, with mean volumes of 36.06 m3, 30.03 m3 and 27.06 m3, respectively (p-values were 0.1834 for A vs. Ba; 0.2009 for Ba vs. C; and 0.0763 for A vs. Cb), and mean basal areas of 1.931 m2, 1.755 m2 and 1.630 m2 for Ba, A and Cb, respectively (p-values were 0.1591 for A vs. Ba; 0.1562 for Ba vs. C; and 0.0724 for A vs. Cb). Th e number of dead trees was signifi cantly higher in cluster A, followed by clusters Cb and Ba, in which mor- tality was quite low, the mean number of dead trees per plot being 11.00, 1.33 and 1.22, respectively (p-values were 0.9889 for A vs. Ba; 0.8768 for A vs. Cb; and 0.0545 for Ba vs. C). Conversely, the occurrence of E. edulis individuals of was highest in cluster A, followed by Ba and Cb, the mean number of individuals per plot being 3.0, 0.36 and 0, respectively (p-values were 0.6939 for A vs. Ba; 0.5598 for A vs. Cb; and 0.3177 for Ba vs. Cb). Th ese results support our fi eld observation that the plots of cluster Cb (comprising plots on the Caverna trail plus plot 3 on the Bugio trail) received more infl uence from human disturbance than did those of the other clusters (Fig. 1) and therefore exhibited less species richness, den- sity and biomass, probably because they are close to areas of intense traffi c (visitor trails and/or houses of traditional peoples). In contrast, the plots of cluster Ba, which had more biomass, are mostly located on the distant and little used Bugio trail. We also observed that cluster Ba exhibi- ted a small number of dead trees in comparison with the other two clusters. Cluster A had less biomass than did cluster Ba but exhibited the highest density, richness and number of dead trees. Our fi ndings are in agreement with the intermediate disturbance hypothesis (Connel 1978), in which extreme levels of disturbance might explain the loss of richness (intense and frequent disturbances in cluster Cb; and less frequent disturbances in cluster Ba). Th e large quantity of dead trees found in cluster A might be considered an inter- mediate disturbance: the opening of clearings might enable the establishment of young and mainly pioneer individuals (Bongers, et al. 2009), thereby increasing species richness. In fact, most of the species within cluster Cb (Fig. 6) were pioneers, whereas most of those within cluster Ba were non- -pioneers. In a 10-year study carried out in French Guiana, Molino & Sabatier (2001) collected evidence to support the intermediate disturbance hypothesis. However, Bongers et al. (2009), in a study of forests in Ghana, found that this hypo- thesis, although applicable to tropical forests and especially dry forests, explains little of the diversity in humid forests. In our study, it was not possible to determine the infl uence of intermediate disturbance on the maintenance of diversity in the canopy. However, it is clear that a relationship exists between tree mortality and the diversity of woody species. Th e Pearson’s correlation tests indicated a correlation between the number of E. edulis individuals and species richness (R2=0.5833, p=0.0199), as well as between the number of E. edulis individuals and the number of dead trees (R2=0.5585, p=0.0002). However, but a smaller corre- lation between density and number of E. edulis individuals (R2=0.2658, p>0.0001). Th erefore, the occurrence of E. edulis is related to species richness and adult tree mortality and the consequent formation of clearings. E. edulis is a non-pioneer, endangered species that commonly occurs in dense rain forests (Mamede et al. 2004; Ramos et al. 2011; Guilherme et al. 2004). Nakazono et al. (2001) observed that young E. edulis individuals grew better under intermediate light conditions than under closed canopy or full sunlight, and suggested that this species might benefi t from the for- mation of clearings. Other authors also observed a positive relationship between canopy openness and survival of E. edulis seedlings, survival rates being higher in clearings than under closed canopies. Table 4. Comparison across studies conducted in protected areas of dense rain forest in southeastern Brazil, in terms of the proportional distribution of species by ecological group. Ecological group Rochelle et al. (2011) Rochelle et al. (2011) Catharino et al. (2005) Catharino et al. (2005) Current study Disturbed area Preserved area Secondary forest Mature forest % species % species % species % species % species % individuals Pioneer sensu lato* 62 22 44-54 35-48 27 26 Non-pioneer sensu lato** 18 65 45-51 49-62 59 61 Uncategorized 20 13 14 13 *Pioneer+early secondary; **late secondary+climax. Acta bot. bras. 27(1): 180-194. 2013. Eliana Cardoso-Leite, Diego Sotto Podadera, Juliana Cristina Peres and Ana Carolina Devides Castello 192 Final remarks Th e forest fragment under study presents three structu- rally and fl oristically distinct conditions: one in which there is low biomass, low density and low species richness, with signs of human disturbance; another in which there is an intermediate quantity of biomass, higher adult mortality, higher density and higher species richness, with signs of intermediate natural disturbance; and a third in which there is even greater biomass, intermediate species richness and no sign of disturbance. Th e species C. contracta, R. jasmi- noides, M. defl exa, P. ambigua and M. uleana can be used as indicators to monitor the condition of mature forest with little disturbance. Th e species E. edulis, C. oblongifolia, P. gla- brata and G. nigrescens can be used as indicators to monitor the condition of mature forest with intermediate natural disturbance. Th e species A. colubrina, A. edulis, C. sylvestris, M. aculeatum, P. gonoacantha, P. crucis and S. multijuga can be used as indicators of the condition of young forest with human disturbance. E. edulis, a common species in dense Figure 4. Cluster analysis with the unweighted pair group method with arithmetic mean (UPGMA), using a matrix of sampling units and total species number. Jacupiranga Complex – Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). A – on the Araçá trail; B – on the Bugio trail; C – on the Caverna trail. Figure 5. Principal components analysis using a matrix of sampling units and number of individuals per species (selecting species with 10 or more individuals). Jacupiranga Complex – Caverna do Diabo State Park and Quilombos do Médio Ribeira Environmentally Protected Area (from 24°20’S to 24°46’S and from 48°03’W to 48°40’W). Dead – dead trees; See Table 1 for other abbreviations. Acta bot. bras. 27(1): 180-194. 2013. Analysis of fl oristic composition and structure as an aid to monitoring protected areas of dense rain forest in southeastern Brazil 193 rain forest studies, exhibited a small number of individuals at our study site and occurred in areas in which there were numerous clearings created by fallen trees. Due to the redefi nition of the boundaries of the former Jacupiranga State Park, our sampling units were located partly within the Caverna do Diabo State Park and partly within the Quilombos do Médio Ribeira Environmentally Protected Area. Because these conservation units have very diff erent land use restrictions, it is important to monitor the conditions of the dense rain forest and analyze the population dynamics of the endangered species in these two preserves. Our data could be used in order to create a baseline for such monitoring. Acknowledgments Th is study received fi nancial support from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, São Paulo Research Foundation; Grant no. 2007/52373). Th e authors would like to thank the Forest Institute, the Forest Foundation, the regional offi ces of Vale do Ribeira State Park and the managers of Caverna do Diabo State Park. Th e authors are also grateful to Dr. Ingrid Koch and Dr. Fiorella Fernanda Mazine Capelo for assisting in the identifi cation of some botanical families. References Aidar, M.P.M.; Godoy, J.R.L. & Bergmann, J. 2001. Atlantic Forest sucession calcareous soil, Parque Estadual Turístico do Alto Ribeira- PETAR, SP. 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