ABSTRACT

This study aims at determining and differentiating the floristic groups of a Deciduous Seasonal Forest’s arboreal component, located on the ridge of the Southern Plateau, in Southern Brazil. Individuals with diameter at breast height ≥ 5.0 cm were sampled in sixty-two plots measuring 10 m × 10 m, which were systematically installed in the forest. Three floristic groups were found: Middle Stage, including 54 species, with Casearia sylvestris as an indicator species; Advanced Stage, with 38 species and Pilocarpus pennatifolius as the indicator species; and Altered Forest, with 27 species and Apuleia leiocarpa, Helietta apiculata, and Machaerium paraguariense as indicator species. A higher proportion of climax light-demanding individuals was reported in the Middle Stage and Altered Forest groups, contrasting with the Advanced Stage group, in which climax shade-tolerant species were predominant. In addition, the groups were differentiated according to their dispersion strategy, with specific syndromes occurring in each group (Middle Stage: zoochory; Advanced Stage: autochory; Altered Forest: anemochory).

Keywords:
cluster analysis; indicator species; spatial distribution

1. INTRODUCTION

The replacement of forests by other forms of land occupation, such as agricultural crops and pastures, as well as the disorderly exploitation of timber and non-timber products, has diminished the natural resources available for use by the human population. The environmental functions of forests have also been adversely affected, such as maintenance of soil productive capacity and water quality in river basins.

The Deciduous Seasonal Forest of Rio Grande do Sul, the primary forest typology of that state (23.8% of the natural forests), partakes in this situation (Rio Grande do Sul, 2002Rio Grande do Sul. Inventário florestal contínuo do Rio Grande do Sul. 2002 [cited 2015 Sept. 1]. Available from: Available from: http://coralx.ufsm.br/ifcrs/frame.htm
http://coralx.ufsm.br/ifcrs/frame.htm... ). The forest’s remnants, despite their range and significance, are actively threatened by rural and urban development (Kilca & Longhi, 2011Kilca RV, Longhi SJ. A composição florística e a estrutura das florestas secundárias no rebordo do Planalto Meridional. In: Schumacher MV, Longhi SJ, Brun EJ, Kilca RV, organizadores. A floresta estacional subtropical: caracterização e ecologia no rebordo do Planalto Meridional. Santa Maria: Pallotti; 2011. p. 53-83.). This condition evidences the need for studies that determine these forests’ ability to support sustainable farming or the need to recover certain ecosystems.

Information on floristic composition, vegetation structure, and relationships between vegetation and the environment were contemplated by Scipioni et al. (2012Scipioni MC, Longhi SJ, Brandelero C, Pedron FA, Reinert DJ. Análise fitossociológica de um fragmento de floresta estacional em uma catena de solos no Morro do Cerrito, Santa Maria, RS. Ciência Florestal 2012; 22(3): 457-466. 10.5902/198050986614
https://doi.org/10.5902/198050986614... ) and Turchetto et al. (2017Turchetto F, Araujo MM, Callegaro RM, Griebeler AM, Mezzomo JC, Berghetti ALP et al. Phytosociology as a tool for forest restoration: a study case in the extreme South of Atlantic Forest Biome. Biodiversity and Conservation 2017; 26(6): 1463-1480. 10.1007/s10531-017-1310-3
https://doi.org/10.1007/s10531-017-1310-... ) regarding remnants of Deciduous Seasonal Forest located on the ridge of the Southern Plateau. However, existing data concerning the western portion of the Plateau is scarce, especially when considering hillside forests and floristic differentiation studies within a fragment, since hillside environments have not been the focus of research in the region.

The differentiation of communities into a forest fragment can be conducted by cluster analysis, which aims at gathering objects into homogeneous groups. The formation of distinct groups suggests the need for differentiated sustainable management in the forest. Similarly, knowledge of indicator species may foster future efforts of preservation and restoration (Marangon et al., 2016Marangon GP, Felker RM, Zimmermann APL, Ferreira RLC, Silva JAA. Análise de agrupamento de espécies lenhosas da Caatinga no estado do Pernambuco. Pesquisa Florestal Brasileira 2016; 36(88): 347-353. 10.4336/2016.pfb.36.88.1030
https://doi.org/10.4336/2016.pfb.36.88.1... ).

In this context, this study aimed at determining and differentiating floristic groups of the arboreal component of a Deciduous Seasonal Forest located in the western region of the Southern Plateau ridge of Rio Grande do Sul.

2. MATERIAL AND METHODS

A fragment of a Submontane Deciduous Seasonal Forest (IBGE, 2012Instituto Brasileiro de Geografia e Estatística - IBGE. Manual técnico da vegetação brasileira. 2nd ed. Rio de Janeiro: IBGE; 2012.), with an area of 10.5 ha, located in the municipality of Jaguari, Rio Grande do Sul, at coordinates 29º24’12” South and 54º38’06” West was assessed. According to the climatic Köppen classification, the region is considered of Cfa (subtropical) climate (Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 2013; 22(6): 711-728. 10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0... ), and the municipality’s average annual precipitation is of 1,879 mm (Machado & Freitas, 2005Machado JLF, Freitas MA. Projeto mapa hidrogeológico do Rio Grande do Sul: relatório final. Porto Alegre: CRPM; 2005.).

The forest is situated in the western portion of the Southern Plateau ridge of Rio Grande do Sul, in an area with a steeply undulating relief (between 190 m and 260 m) and a predominantly western exposure, where the maximum slope is 40° (89%). Regosols and leptosols predominate in the area and exhibit lithic contact relatively close to the surface (Pedron & Dalmolin, 2011Pedron FA, Dalmolin RSD. Solos da região do rebordo do Planalto Meridional no Rio Grande do Sul. In: Schumacher MV, Longhi SJ, Brun EJ, Kilca RV, organizadores. A floresta estacional subtropical: caracterização e ecologia no rebordo do Planalto Meridional. Santa Maria: Pallotti; 2011. p. 33-51.).

Five parallel sample strips were systematically installed from the base (west) to the top of the hill (east), approximately 50 m apart and with variable length (Figure 1). The sample area included the stretch of the forest fragment located inside a rural property that exhibited better conditions of preservation (3.8 ha), disregarding the section with visually more noticeable change. The second northernmost sampling range had an interruption due to the presence of rocky outcrop. The sampling strips were divided into contiguous plots with dimensions of 10 m × 10 m (100 m²), totaling 62 plots (0.62 ha of sample area). During the second semester of 2010 and the first half of 2011, all individuals with diameter at breast height (DBH) ≥ 5.0 cm in the plots were identified and measured.

Botanical material of unidentified species was collected for analysis and identification in the Herbarium of the Department of Forest Sciences of Universidade Federal de Santa Maria. In order to update and confirm the nomenclature of the species and their respective authors, the Flora do Brasil 2020 catalog was utilized (Forzza et al., 2018Forzza RC, Costa AF, Walter BMT, Bicudo C, Moura CWN, Peralta DF et al. Flora do Brasil 2020. 2018 [cited 2018 Feb. 18]. Available from: Available from: www.floradobrasil.jbrj.gov.br/
www.floradobrasil.jbrj.gov.br/... ). Family delimitation followed the Angiosperm Phylogeny Group IV classification system (Byng et al., 2016Byng JW, Chase MW, Christenhusz MJM, Fay MF, Judd WS, Mabberley DJ et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society 2016; 181(1): 1-20. 10.1111/boj.12385
https://doi.org/10.1111/boj.12385... ).

Sampling adequacy was verified using the species accumulation curve generated with the PC-ORD 4.41 program (McCune & Mefford, 1999McCune B, Mefford MJ. PC-ORD: multivariate analysis of ecological data. Version 4.41. Gleneden Beach: MjM Software; 1999.). The plots were grouped based on the abundance of the species, using the agglomerative hierarchical method, with Ward attachment, and the Euclidian distance as a measure of dissimilarity. The data were organized in spreadsheets with 62 lines (sampled plots) and 57 columns (sampled species), and the cluster analysis was processed using the SPSS 13.0 program for Windows (SPSS, 2004Statistical Package for the Social Sciences - SPSS. SPSS. Version 13.0. Chicago: SPSS; 2004.).

The formed clusters were differentiated by the occurrence of species, floristic similarity, analysis of indicator species, aggregation, successional group, and species dispersion strategy. The floristic similarity between the groups was obtained using the Jaccard index, which is based on the presence or absence of species, and ranges from 0 to 1, where 1 indicates maximum floristic similarity between the compared areas (e.g., forests, clusters, and plots). In other words, all species that belonged to a sample also belonged to another sample (Souza & Soares, 2013Souza AL, Soares CPB. Florestas nativas: estrutura, dinâmica e manejo. Viçosa: Editora UFV; 2013.).

Indicator species analysis (ISA) was employed to verify the species that characterize the floristic groups. The method provides the indicator value (IV) for each species in each group, with the statistical significance of the IV verified by the Monte Carlo test, which retained 500 iterations in this study. Such analysis, performed in the PC-ORD 4.41 program, utilized a matrix containing the abundance of species in the plots in each floristic group (Kent, 2012Kent M. Vegetation description and data analysis: a pratical approach. 2nd ed. Cichester: Wiley-Blackwell; 2012.; McCune & Mefford, 1999McCune B, Mefford MJ. PC-ORD: multivariate analysis of ecological data. Version 4.41. Gleneden Beach: MjM Software; 1999.; Valentin, 2012Valentin JL. Ecologia numérica: uma introdução à análise multivariada de dados ecológicos. Rio de Janeiro: Interciência; 2012.).

The spatial distribution pattern (aggregation) of the species was assessed using the Payandeh index (Pi), determined in three classes (Souza & Soares, 2013Souza AL, Soares CPB. Florestas nativas: estrutura, dinâmica e manejo. Viçosa: Editora UFV; 2013.): random (Pi ≤ 1.0), tend to aggregate (1.0 < Pi ≤ 1.5), and aggregated (Pi > 1.5). In this analysis, species with one sampled individual were disregarded, given they exhibited a non-aggregated (random) distribution, a procedure also adopted by Watzlawick et al. (2011Watzlawick LF, Albuquerque JM, Redin CG, Longhi RV, Longhi SJ. Estrutura, diversidade e distribuição espacial da vegetação arbórea na floresta ombrófila mista em sistema faxinal, Rebouças (PR). Ambiência 2011; 7(3): 415-427. 10.5777/ambiencia.2011.03.01
https://doi.org/10.5777/ambiencia.2011.0... ) and Nascimento et al. (2001Nascimento ART, Longhi SJ, Brena DA. Estrutura e padrões de distribuição espacial de espécies arbóreas em uma amostra de floresta ombrófila mista em Nova Prata, RS. Ciência Florestal 2001; 11(1): 105-119. 10.5902/19805098499
https://doi.org/10.5902/19805098499... ). When one species presented in more than one floristic group, the Payandeh index was calculated in the groups where the species had two or more individuals sampled.

The species were classified into successional groups, according to Swaine & Whitmore (1988Swaine MD, Whitmore TC. On the definition of ecological species groups in tropical rain forests. Vegetatio 1988; 75(1-2): 81-86. 10.1007/BF00044629
https://doi.org/10.1007/BF00044629... ) and Oliveira-Filho et al. (1994Oliveira-Filho AT, Vilela E, Carvalho DA, Gavilanes ML. Effects of soils and topography on the distribution of tree species in a tropical riverine forest in south-eastern Brazil. Journal of Tropical Ecology 1994; 10(4): 483-508. 10.1017/S0266467400008178
https://doi.org/10.1017/S026646740000817... ): pioneers (P), climax light-demanding (CL), and climax shadow-tolerant (CS). The former group requires full solar luminosity in regeneration, growth, development, and survival processes. Light-demanding climatic species can germinate under shade, but young plants need abundant light to grow and reach the canopy and maturity. In turn, shade-tolerant species can develop under shading, and reach maturity at the canopy or beforehand.

As for the dispersion strategy, the species were classified into three categories, according to Pijl (1972Pijl LVD. Principles of dispersal in higher plants. Berlin: Springer-Verlag; 1972.): zoochorous, anemochorous, and autochorous. Zoochorous species are dispersed by animals and have attractive and/or alimentary diaspores, as well as diaspores with adhesive structures, such as hooks and bristles. Anemochorous species have diaspores with structures that provide wind dispersion (winged, feathery, or balloon-shaped). Autochorous species, on the other hand, do not fit into the two previous categories, presenting dispersion by gravity and explosion.

The successional group (P, CL, and CS) and the dispersion strategy (zoochory, anemochory, and autochory) were determined by bibliographic consultation. When the species exhibited different classification in the literature, field observations and researcher consultations were carried out.

3. RESULTS AND DISCUSSION

The species accumulation curve indicated that the sample was sufficient to represent the studied vegetation, given a tendency towards stabilization was observed (Figure 2). Such a trend was evidenced at the final portion of the curve, in which the 10% increase in the sample area resulted in an increment in new species of less than 5%, a condition mentioned by Kersten & Galvão (2011Kersten RA, Galvão F. Suficiência amostral em inventários florísticos e fitossociológicos. In: Felfili JM, Eisenlohr PV, Melo MMRF, Andrade LA, Meira-Neto JAA, editores. Fitossociologia do Brasil: métodos e estudos de caso. Viçosa: Editora UFV; 2011. p. 156-173.) as necessary to determine the minimum sample area.

A total of 1,107 individuals were sampled in the tree stratum, pertaining to 57 species and 25 botanical families (Table 1). The dendrogram generated by the cluster analysis (Figure 3) indicated the presence of three groups: Group 1 (36 plots), Group 2 (18 plots), and Group 3 (8 plots). The Group 1 was referred to as the Middle Stage, while Group 2 was denominated the Advanced Stage, and Group 3 the Altered Forest. These designations were applied to approximate the reality of the clusters with the floristic properties of forests in different stages or preservation conditions. Therefore, the aspects observed in the study area and the characteristics of the indicator species determined by ISA were considered.

In the ISA, the species that retained a significant observed indicator value (OIV) in the Monte Carlo test (p-value < 0.05) were considered as group indicators. Only five of the 57 observed species were deemed as group indicators: in the Middle Stage group, Casearia sylvestris Sw. (OIV = 39.0; p = 0.04); in Advanced Stage, Pilocarpus pennatifolius Lem. (OIV = 89.7; p = 0.02), and in Altered Forest, Apuleia leiocarpa (Vogel) J.F.Macbr. (OIV = 45.0; p = 0.02), Helietta apiculata Benth. (OIV = 89.9; p = 0.02), and Machaerium paraguariense Hassl. (OIV = 34.8; p = 0.02).

The species Casearia sylvestris is considered climax light-demanding and generalist regarding environmental conditions, occurring in several types of soils, from low to high chemical fertility, wet or dry, and from sandy to clayey texture (Carvalho, 2007Carvalho PER. Cafezeiro-do-mato: Casearia sylvestris. Colombo: Embrapa Florestas; 2007.; Scipioni et al., 2013Scipioni MC, Galvão F, Longhi SJ. Composição florística e estratégias de dispersão e regeneração de grupos florísticos em florestas estacionais deciduais no Rio Grande do Sul. Floresta 2013; 43(2): 241-254. 10.5380/rf.v43i2.27098
https://doi.org/10.5380/rf.v43i2.27098... ). In addition, Reitz et al. (1988Reitz R, Klein RM, Reis A. Projeto Madeira do Rio Grande do Sul. Porto Alegre: SUDESUL; 1988.) emphasized that the species also develops in rocky and shallow soils. Thus, its occurrence is explained as being an indicator of the Middle Stage group, which included plots with different environmental conditions.

In the Advanced Stage group, the occurrence of Pilocarpus pennatifolius (tolerant to shade) as an indicator species evidences that the forest structure provided shading conditions that were favorable to the development of a dense population, with an incidence of the species in all plots of the group. Also, the preference of this species is associated to the group by its form of dispersion (autochory), which, according to Giehl et al. (2007Giehl ELH, Athayde EA, Budke JC, Gesing JPA, Einsiger SM, Canto-Dorow TS. Espectro e distribuição vertical das estratégias de dispersão de diásporos do componente arbóreo em uma floresta estacional no sul do Brasil. Acta Botanica Brasilica 2007; 21(1): 137-145. 10.1590/S0102-33062007000100013
https://doi.org/10.1590/S0102-3306200700... ), is effective only for diaspore displacement at short distances and, therefore, hinders the spread of propagules to larger areas.

The preference of the species Apuleia leiocarpa, Helietta apiculata, and Machaerium paraguariense regarding the Altered Forest group is due to environmental characteristics, such as proximity to the edge of the forest, which favored the emergence of these species, classified as climax light-demanding. Moreover, the significant surface stoniness verified in the area possibly acted as a limiting ecological factor for the establishment of other species, but was tolerated by the three indicator species of the group. Such conditions were mentioned by Lorenzi (2008Lorenzi H. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas do Brasil. 5th ed. Nova Odessa: Instituto Plantarum; 2008.) when describing the environment where the species Machaerium paraguariense preferably occurs: in secondary forests and almost always in high rocky terrains, where drainage is swift.

The indicator species of the Altered Forest group are classified as anemochorous, which partially explains their high abundance. This syndrome is favored in more open forests that lack a continuous canopy (Howe & Smallwood, 1982Howe FH, Smallwood J. Ecology of seed dispersal. Annual Review of Ecology and Systematics 1982; 13: 201-228. 10.1146/annurev.es.13.110182.001221), as observed in some points in the area. According to Morellato & Leitão Filho (1992Morellato LPC, Leitão Filho HF. Padrões de frutificação e dispersão na Serra do Japi. In: Morellato LPC, organizador. História natural da Serra do Japi: ecologia e preservação de uma área florestal no Sudeste do Brasil. Campinas: Editora Unicamp; 1992. p. 111-140.), the presence of emergent arboreal individuals associated with forest deciduousness may enhance the dispersion of anemochorous diaspores, influencing forest structure.

The majority of the species sampled in the forest occurred in the Middle Stage group (53 species = 93% of the total), with the most abundant species being Annona neosalicifolia (50 individuals), Casearia sylvestris (44), Gymnanthes klotzschiana (41), Actinostemon concolor (38), and Myrocarpus frondosus (38). In the Advanced Stage group, 38 species (67% of the total) were observed, with Pilocarpus pennatifolius as the most significant, with 164 individuals, followed by Annona neosalicifolia (20), Myrocarpus frondosus (18), and Casearia sylvestris (14). In the Altered Forest group, the species Helietta apiculata (63), Machaerium paraguariense (45), Sebastiania brasiliensis (19), and Apuleia leiocarpa (12) retained the most substantial number of individuals among the 27 species found in the group (Table 1). The differences in richness may be related to the larger sample area attributed to the Middle Stage when compared to the other groups.

The Jaccard similarity index indicated that the Middle and Advanced Stage groups were more similar among each other (Jaccard = 0.60; 34 species in common) and that the lowest floristic similarity was verified between the Middle Stage and Altered Forest groups (0.48). The Advanced Stage and Altered Forest groups retained an index of 0.55. The difference in similarity is related to the presence or absence of the species in the groups. Twenty-two species, including Helietta apiculata, Machaerium paraguariense, Myrocarpus frondosus, Pilocarpus pennatifolius, and Sebastiania brasiliensis, were found in all three groups. In contrast, Banara tomentosa and Ruprechtia laxiflora and Cedrela fissilis and Sideroxylon obtusifolium occurred only in the Middle and Advanced Stages, respectively, while species exclusivity was not observed in the Altered Forest group.

In order to determine the degree of species aggregation, by means of the Payandeh index, 42, 24, and 14 species were considered for the Middle Stage, Advanced Stage and Altered Forest groups, respectively (Figure 4). An aggregated pattern was predominant in the arboreal stratum, indicating that most species tend to form population densities in specific areas.

The species Gymnanthes klotzschiana (8.29), Annona neosalicifolia (7.38), Myrocarpus frondosus (6.38), and Eugenia uniflora (5.50) were significantly aggregated in the Middle Stage group, and, in the Advanced Stage group, Schaefferia argentinensis (3.67) exhibited a higher aggregation index. In turn, the Altered Forest group retained higher values of aggregation of Machaerium paraguariense (11.68) and Sebastiania brasiliensis (4.32). The more significant aggregation of these species may be influenced by more favorable habitat conditions, such as landform and availability of light and water, species autoecology, and different rates of mortality and recruitment (Capretz et al., 2012Capretz RL, Batista JLF, Sotomayor JFM, Cunha CR, Nicoletti MF, Rodrigues RR. Padrão espacial de quatro formações florestais do estado de São Paulo, através da função K de Ripley. Ciência Florestal 2012; 22(3): 551-565. 10.5902/198050986622
https://doi.org/10.5902/198050986622... ; Crawley, 1986Crawley MJ. Plant ecology. Oxford: Blackwell Scientific Publications, 1986.; Silva et al., 2012Silva KE, Martins SV, Santos NT, Ribeiro CAAS. Padrões espaciais de espécies arbóreas tropicais. In: Martins SV, editor. Ecologia de florestas tropicais do Brasil. 2nd ed. Viçosa: Editora UFV; 2012. p. 216-244.).

The spatial pattern of some species was distinct between the groups. For example, Gymnanthes klotzschiana (Middle Stage group = 8.29 - aggregated; Advanced Stage group = 0.94 - not aggregated) and Machaerium paraguariense (Middle Stage = 1.57 - grouped; Advanced Stage = 1.35 - tend to aggregate; Altered Forest group = 11.68 - aggregated) occurred in a different manner. The strongly aggregated pattern of Gymnanthes klotzschiana in the Middle Stage group may be related to water influence, due to the presence of water bodies adjacent to some plots. According to Silva et al. (2012Silva KE, Martins SV, Santos NT, Ribeiro CAAS. Padrões espaciais de espécies arbóreas tropicais. In: Martins SV, editor. Ecologia de florestas tropicais do Brasil. 2nd ed. Viçosa: Editora UFV; 2012. p. 216-244.), such pattern occurs due to the greater tolerance of the species to soils with water excess, which favors recruitment.

Considering the succession categories, it was verified, regarding the totality of the forest, that the CL species occurred in a greater number of individuals (57% of the total forest individuals) and species (63% of the total species of the forest), followed by CS (34% and 23%, respectively) and P (5% and 11%) species (Table 2).

Regarding the number of species, the three groups had a forest-like pattern, with greater CL richness, followed by CS and P. Similar results were reported by Scipioni et al. (2013Scipioni MC, Galvão F, Longhi SJ. Composição florística e estratégias de dispersão e regeneração de grupos florísticos em florestas estacionais deciduais no Rio Grande do Sul. Floresta 2013; 43(2): 241-254. 10.5380/rf.v43i2.27098
https://doi.org/10.5380/rf.v43i2.27098... ) and Callegaro et al. (2014Callegaro RM, Araujo MM, Longhi SJ. Fitossociologia de agrupamentos em Floresta Estacional Decidual no Parque Estadual Quarta Colônia, Agudo-RS. Agrária 2014; 9(4): 590-598. 10.5039/agraria.v9i4a4853
https://doi.org/10.5039/agraria.v9i4a485... ) in the same forest type, where light-demanding climactic species retained larger proportions of individuals and species. The higher floristic representativity of these species was also observed by Abreu et al. (2014Abreu TAL, Pinto JRR, Mews HA. Variações na riqueza e na diversidade de espécies arbustivas e arbóreas no período de 14 anos em uma Floresta de Vale, Mato Grosso, Brasil. Rodriguésia 2014; 65(1): 73-88.), in a Semi-Deciduous Seasonal Forest located in the Chapada dos Guimarães National Park, who attributed this condition to canopy discontinuity due to the valley’s rugged relief.

The Middle Stage and Altered Forest groups had a more substantial number of individuals pertaining to the successional CL category, contrasting with the Advanced Stage, where more CS individuals occurred. Such condition can be explained by the abundance of the species Pilocarpus pennatifolius, which is a known indicator of the Advanced Stage group, classified as climax shadow-tolerant.

The analyzed forest was primarily composed of species with zoochorous dispersion (67%), a result similar to other forests surveyed in several regions of Brazil, such as the Seasonal Forest in Querência, MT (Stefanello et al., 2010Stefanello D, Ivanauskas NM, Martins SV, Silva E, Kunz SH. Síndromes de dispersão de diásporos das espécies de trechos de vegetação ciliar do rio das Pacas, Querência - MT. Acta Amazonica 2010; 40(1): 141-150. 10.1590/S0044-59672010000100018
https://doi.org/10.1590/S0044-5967201000... ), the Mixed Ombrophylous Forest in Tijucas do Sul, PR (Liebsch & Acra, 2007Liebsch D, Acra LA. Síndromes de dispersão de diásporos de um fragmento de floresta ombrófila mista em Tijucas do Sul, PR. Revista Acadêmica Ciência Animal 2007; 5(2): 167-175. 10.7213/cienciaanimal.v5i2.9750
https://doi.org/10.7213/cienciaanimal.v5... ), and the Dense Ombrophylous Forest in Rio de Janeiro (Carvalho, 2010Carvalho FA. Síndromes de dispersão de espécies arbóreas de florestas ombrófilas submontanas do estado do Rio de Janeiro. Revista Árvore 2010; 34(6): 1017-1023. 10.1590/S0100-67622010000600007
https://doi.org/10.1590/S0100-6762201000... ). Similarly to the forest fragment as a whole, the three groups retained a more considerable richness of zoochorous species, followed by anemochorous and autochorous individuals.

The groups showed discrepancies when the number of individuals was analyzed: the Middle Stage had zoochory as its main syndrome (54%), the Advanced Stage retained autochory (54%), and the Altered Forest, anemochory (76%). The elevated proportion of individuals of the predominant dispersion syndromes was due to the abundance of some species, namely Pilocarpus pennatifolius (autochorous), with 164 species in the Advanced Stage, Helietta apiculata and Machaerium paraguariense (anemochorous), with 108 individuals in the Altered Forest, and Casearia sylvestris and Annona neosalicifolia (zoochorous), with a total of 94 individuals in the Middle Stage. The numerical predominance of different dispersion strategies in each floristic group evidences that this ecological characteristic was determinant of the differentiation of arboreal communities in the analyzed fragment. Moreover, this result corroborates that of Howe & Smallwood (1982Howe FH, Smallwood J. Ecology of seed dispersal. Annual Review of Ecology and Systematics 1982; 13: 201-228. 10.1146/annurev.es.13.110182.001221), who stated that the prevalence of a specific dispersal mechanism in a given habitat indicates that dispersion agent pressures and physical conditions influenced species selection.

4. CONCLUSIONS

The presence of three floristic groups with distinct indicator species was detected: Middle Stage (Casearia sylvestris); Advanced Stage (Pilocarpus pennatifolius), and Altered Forest (Apuleia leiocarpa, Helietta apiculata, and Machaerium paraguariense). The clusters had a more significant richness of zoochorous species, while the incidence of trees with each dispersion strategy was distinct between the groups, predominating anemochory in the Altered Forest, zoochory in the Middle Stage, and autochory in the Advanced Stage.

The light-demanding climatic species predominated in terms of richness and abundance in the Middle Stage and Altered Forest, while in the Advanced Stage a greater proportion of individuals belonging to the shade-tolerant climatic species was observed. Both aspects used for cluster differentiation showed that the two are floristically and structurally distinct.

ACKNOWLEDGEMENTS

The authors thank the Department of Forest Sciences of Universidade Federal de Santa Maria for the support in data gathering.

REFERENCES

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