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The tree-shrub vegetation in rocky outcrop cerrado areas in Goiás State, Brazil

Abstract

We describe the floristic composition of the tree-shrub vegetation in 10 areas of rocky outcrop cerrado in Goiás State, Brazil. Ten 20×50m plots (totaling 1ha) were established and all of the individuals with diameters at 30cm above soil level (DB30) ³5cm were included in the sampling. Comparative analyses of the flora were realized using similarity indices (Sørensen and Czekanowski), classification analysis (TWINSPAN), and the Mantel test. A total of 13,041 tree-shrub individuals were sampled, distributed among 219 species, 129 genera and 55 families. Fabaceae was the most well-represented family, followed by Myrtaceae, Melastomataceae, Vochysiaceae, Malphigiaceae, and Rubiaceae. Fully 42.3% of the comparisons evaluated by the Sørensen index were >0.50, while all the values were <0.50 for the Czekanowski index, with the exception of Jaraguá and Mara Rosa areas. The TWINSPAN classification generated four divisions and, in general, only the differences in the size of the population were responsible for the groupings. The Mantel test indicated that there was no relationship between floristic similarity and the distances between the areas (r=0.32, P=0.05). It therefore appears that the areas of rocky outcrop cerrado in Goiás State are relatively floristically homogeneous and that they are principally distinguished by the differences in the sizes of the populations of their dominant species, and the presence of exclusive species in certain areas.

biodiversity; Cerrado biome; floristic composition; floristic similarity; rocky outcrops


SYSTEMATICS, PHYLOGENY AND FLORISTICS

The tree-shrub vegetation in rocky outcrop cerrado areas in Goiás State, Brazil

Tassiana Reis Rodrigues dos SantosI;II;* * Corresponding author: tassianatxu@hotmail.com ; José Roberto Rodrigues PintoIII; Eddie LenzaIV; Henrique Augusto MewsI

IPrograma de Pós-Graduação em Ciências Florestais, Universidade de Brasília – UnB, Caixa Postal 04357, 70919-970 Brasília, DF, Brazil.

IICurrent address: Programa de Pós-Graduação em Botânica, UnB, Caixa Postal 04457, 70919-970 Brasília, DF, Brazil.

IIIUniversidade de Brasília, Departamento de Engenharia Florestal, Caixa Postal 04357, 70919-970 Brasília, DF, Brazil.

IVUniversidade do Estado do Mato Grosso – Unemat, Departamento de Ciências Biológicas, Caixa Postal 08, 78690-000 Nova Xavantina, MT, Brazil.

ABSTRACT

We describe the floristic composition of the tree-shrub vegetation in 10 areas of rocky outcrop cerrado in Goiás State, Brazil. Ten 20×50m plots (totaling 1ha) were established and all of the individuals with diameters at 30cm above soil level (DB30) ³5cm were included in the sampling. Comparative analyses of the flora were realized using similarity indices (Sørensen and Czekanowski), classification analysis (TWINSPAN), and the Mantel test. A total of 13,041 tree-shrub individuals were sampled, distributed among 219 species, 129 genera and 55 families. Fabaceae was the most well-represented family, followed by Myrtaceae, Melastomataceae, Vochysiaceae, Malphigiaceae, and Rubiaceae. Fully 42.3% of the comparisons evaluated by the Sørensen index were >0.50, while all the values were <0.50 for the Czekanowski index, with the exception of Jaraguá and Mara Rosa areas. The TWINSPAN classification generated four divisions and, in general, only the differences in the size of the population were responsible for the groupings. The Mantel test indicated that there was no relationship between floristic similarity and the distances between the areas (r=0.32, P=0.05). It therefore appears that the areas of rocky outcrop cerrado in Goiás State are relatively floristically homogeneous and that they are principally distinguished by the differences in the sizes of the populations of their dominant species, and the presence of exclusive species in certain areas.

Keywords: biodiversity, Cerrado biome, floristic composition, floristic similarity, rocky outcrops

INTRODUCTION

The Cerrado (Brazilian cerrado) biome originally occupied approximately 2,000,000km² (22%) of the country (Oliveira Filho & Ratter 2002, Ribeiro & Walter 2008), but its area has been reduced over the years to only 60.5% of its original extent (Sano et al. 2009). The diversified phytophysiognomic mosaic of Cerrado includes open field formations characterized by herbaceous plants (principally grasses), cerrado formations characterized by grasses with scattered and thin trees and sub-arboreal plants, and forest formations dominated by arboreal species (Ribeiro & Walter 2008). According to Sano et al. (2009), approximately 61% of the natural areas of Cerrado are cerrado formations, 32% are forest formations, while 7% are open herbaceous areas.

One of the principal phytophysiognomic types of the biome is cerrado sensu stricto, the category classified as cerrado, which demonstrates well-defined arboreal and shrub-herbaceous layers (Ribeiro & Walter 2008) with arboreal coverage varying from 10% to 60% (Eiten 1992). According to Ribeiro & Walter (2008), cerrado sensu stricto can be divided into four subtypes depending on the density of the tree-shrub component and local environmental conditions: dense cerrado, typical cerrado locally called cerrado típico, thin cerrado, and rocky outcrop cerrado locally called "cerrado rupestre".

Rocky outcrop cerrados generally occurs in environments with rock outcrops (Ribeiro & Walter 2008) with predominantly shallow, poorly evolved and litholic neosols, with the A horizon lying directly on the rock surface, or with a very thin C horizon (Reatto et al.

2008). The root systems of the plants growing there cannot penetrate very deeply, so that woody individuals are predominately found in cracks and crevices that have accumulated larger volumes of substrate (Romero 2002, Reatto et al. 2008). The rocky outcrop cerrado vegetation is characterized by tree-shrub species with heights between 2 and 4m covering between 5% and 20% of the surface; the subshrub-herbaceous layer is thin, with species typical of this vegetation type (Ribeiro & Walter 2008).

Rocky outcrop cerrados cover approximately 6.6% of Goiás and are distributed throughout the state (Lima 2008), but only limited studies have been conducted in this important phytophysiognomy of the Cerrado biome (Manoel 1999, Amaral et al. 2006, Miranda et al.

2007, Moura et al. 2007, 2010, Pinto et al. 2009, Lima et al. 2010), and is still little-known and incompletely explored scientifically. Studies of floristic composition furnish basic information for understanding different plant formations and are essential for subsequent detailed studies (Van den Berg & Oliveira Filho 2000).

We describe here the floristic composition of the tree-shrub vegetation in 10 areas of rocky outcrop cerrado in Goiás State, Brazil, present a checklist of the species that can be used to evaluate the contributions of the different taxa and the floristic composition of these environments, and evaluate the floristic similarities between the areas surveyed. To that end, we have assumed that the rocky outcrop cerrado is a differentiated environment, principally in relation to its edaphic conditions: poor and thin soils with low pH and high concentrations of exchangeable aluminum (Benites et al. 2003, Reatto et al. 2008) – and should therefore demonstrate a unique floristic composition. In addressing these objectives, the following questions were formulated: What tree-shrub species grow in the rocky outcrop cerrado areas of Goiás State? Does the rocky outcrop cerrado in that area contain an elevated floristic richness of tree-shrub species? Are the study areas floristically similar? Is the tree-shrub vegetation of this phytophysiognomy composed of generalist species or species specialized for a specific habitat?

MATERIAL AND METHODS

Study area – The current study was undertaken in 10 areas of rocky outcrop cerrado in Goiás State (GO), in the central western region of Brazil (figure 1) (12°23'46" to 19°29'42"S and 45°58'36" to 53°14'53"W). The regional climate is type Aw by the Köppen classification system, and is characterized by dry winters and rainy summer seasons, with annual average temperatures varying from 18°C to 26°C and annual precipitation rates oscillating between 1,200 and 2,500mm (Sieg 2009). The highest elevation in the state is Morro Alto in the region of Chapada dos Veadeiros (approximately 1,921m), while the lowest altitudes are found in the Araguaia region (approximately 182m) (Sieg 2009) (table 1). Litholic neosols, upon which rocky outcrop cerrado vegetation normally develops, occupy approximately 8% of the state (Sano et al. 2006).


According to Lima (2008), rocky outcrop cerrado areas cover approximately 6.6% of Goiás State. These areas occur throughout the state, with greater frequency in the northeast in the micro-regions of Chapada dos Veadeiros, in the northern section of Brasília and Porangatu neighborhood. The present study surveyed areas in different regions where rocky outcrop cerrado occurs in Goiás State: in the northeast (three areas), southeast (two areas), southwest (two areas), and central region (three areas). The northwestern region of the state was excluded as there are few records of rocky outcrop cerrado there (Lima 2008).

Vegetation survey – We established ten 20×50m plots, totaling 1ha for each site, in each of the 10 areas inventoried, following the protocols established for the Network of Permanent Plots in the Cerrado and Pantanal Biomes (Felfili et al. 2005). All the individuals with diameter 30cm above soil level (DB30) ³5cm were considered tree-shrub plants and included in the sampling, as recommended by Felfili et al. (2005). The botanical identifications were made in the field and by consulting the specific appropriate literature and herbaria samples stored at the Universidade de Brasília and Instituto Brasileiro de Geografia e Estatística, as well as specialists. The APG III (2009) classification system was adopted for the botanical families. The revision and updating of the taxa names was performed following Forzza et al. (2010). The classification of the species as well as their habits (the characteristics or appearances of plants: vines, subshrubs, shrubs, treelets, and trees) followed Mendonça et al. (2008).

Data analysis – The qualitative Sørensen index (Brower & Zar 1977) and the quantitative Czekanowski index (Kent & Coker 1992) were used to analyze the floristic similarities among the 10 areas inventoried. According to Kent & Coker (1992), the Sørensen and Czekanowski index values vary between zero and one, with values greater than 0.5 indicating high similarities between the communities. Additionally, the Mantel test (Legendre & Legendre 1998), using the PC-ORD 4 software program (McCune & Mefford 1999), was used to evaluate if the floristic similarity values generated by the Czekanowski index were related to the geographical distances between the areas. To evaluate the significance of the Mantel test, 1,000 random Monte Carlo permutations were run. TWINSPAN (Kent & Coker 1992) analysis was used to identify divisions and grouping patterns among areas based on floristic characteristics, which indicated and identified the preferential and indicator species of each area.

RESULTS AND DISCUSSION

A total of 13,041 tree-shrub individuals were surveyed, distributed among 219 species, 129 genera, and 55 botanical families; 196 (84.49%) of these taxa were identified to the species level, 17 (7.76%) to the genus level, five (2.28%) to the family level; one plant remained without definitive indication (table 2). In terms of their habits, 113 (57.65%) species were considered trees, 24 (12.24%) shrubs, 18 (9.18%) treelets, 15 (7.65%) trees/shrubs, 13 (6.63%) treelets/shrubs, six (3.06%) subshrubs, five (2.65%) trees/treelets, one (0.51%) shrub/subshrub, and one (0.51%) tree/vine.

According to Mendonça et al. (2008), the Cerrado biome as a whole contains 11,627 species of vascular phanerogams, 4,346 of which are considered tree-shrub. As such, the species recorded in the 10 rocky outcrop cerrado areas sampled here represent approximately 5.03% of all of the tree-shrub species recorded for the entire biome. In terms of the cerrado (sensu lato), these species represent 9.55% of the recorded species, and for the rocky fields (sensu lato) they represent 17.39%. This data indicates the high floristic representivity of the rocky outcrop cerrado vegetation in Goiás State in terms of the tree-shrub components of the cerrado formations of the Cerrado biome. Considering that rocky field environments represent only 6.6% of Goiás State (Lima 2008), their floristic representivity becomes even more apparent.

The local floristic richnesses varied from 61 (in the municipalities of Nazário, Piranhas and Pirenópolis) to 84 species (Mineiros). This range is considered normal among cerrado formations (cerrado sensu stricto), which usually have less than 100 species per hectare (Felfili et al. 2004). The municipality of Mineiros is located in the Paraná Guimarães eco-region proposed by Arruda et al. (2008), with both sedimentary and volcanic rock formations (such as basalt – which is rich in iron/magnesium minerals) (Reatto et al. 2008). According to Benites et al. (2007), areas with rock outcrops can demonstrate considerable edapho-environmental diversity, reflected in vegetation mosaics that are largely determined by the local topography and by micro-environmental aspects. As such, the regional environmental heterogeneity contributed to the high floristic richness observed in Mineiros.

In general, the tree-shrub species richnesses observed in each of the sampling areas was greater than that reported in other studies of rocky outcrop cerrado using similar survey methodologies. A study by Amaral et al. (2006) in the Federal District, for example, reported 51 species, and by Miranda et al. (2007) in the Serra Dourada-GO recorded 54 species, by Pinto et al. (2009) in Cocalzinho, GO (65), by Moura et al. (2007, 2010) in Pirenópolis, GO (56 and 65 species respectively), and studies by Moura (2010) in the Rio Preto State Park, MG, in the Sete Cidades National Park-PI and in Cáceres, MT listed 42, 47 and 69 species respectively. The high richness values encountered in these areas demonstrate the necessity protecting rocky outcrop cerrado sites to ensure the preservation of their unique biodiversity. According to Benites et al. (2007), cerrado/rocky field environments are not suitable for agricultural and are therefore natural refuges for the regional flora and fauna – and should be considered priority areas for biodiversity conservation.

Among the 10 areas sampled, Fabaceae was the most representative plant family in terms of the numbers of species (35), followed by Myrtaceae (18), Melastomataceae (13), Vochysiaceae (12), Malphigiaceae (10), and Rubiaceae (10). The high representivities of these families were likewise observed in other studies of rocky outcrop cerrado sites in Brazil (Manoel 1999, Amaral et al. 2006, Moura et al. 2007, Pinto et al. 2009), as well as in cerrado areas sensu stricto (Marimon et al. 1998, Felfili et al. 2002, Assunção & Felfili 2004), and it could be seen that the rocky field and typical cerrado areas of Goiás State do not differ greatly in terms of their most representative families. Nonetheless, Marcgraviaceae and Velloziaceae, two well-represented families in rocky outcrop cerrados in terms of their numbers of species, densities of individuals, and geographical distribution (table 2), are generally poorly represented in areas of deep soils of cerrado (Ratter et al. 2000, 2003, Bridgewater et al. 2004), thus defining certain floristic differences between typical and rocky outcrop cerrados in the state.

Goodland (1979) considered the family Fabaceae to be one of the most important plant groups in the Cerrado biome. Vochysiaceae was also one of the best represented families in the present study, and its species (e.g. Qualea grandiflora, Q. parviflora, Q. multiflora, Vochysia thyrsoidea and V. elliptica) are known to accumulate aluminum (Haridasan 2000). According to this same author, the families Melastomataceae (e.g. Miconia ferruginata and M. pohliana); Rubiaceae (Palicourea rigida) also accumulate this metal. It is important to note that all the species cited above and identified as aluminum accumulators were encountered in the present study.

The floras of the rocky outcrop cerrado areas analyzed were largely composed of species known from cerrado sensu stricto (cerrado) formations growing on deep soils (74.40%) and forest species (21.50%). Nine species (4.10%) considered specialist to specific habitats (sensu Rabinowitz 1981) of rocky outcrop cerrado and that are restricted to rupestre environments were recorded: Clusia weddelliana, Schwartzia adamantium, Mimosa setosissima, Tibouchina papyrus, Wunderlichia mirabilis, W. cruelsiana, Hyptis pachyphylla (Ratter et al. 2000, Ribeiro & Walter 2008, Pinto et al. 2009), Vellozia variabilis (Silva et al. 2001), and Vellozia tubiflora (Munhoz & Proença 1998). Tibouchina papyrus is important because its distribution is restricted to Goiás State, occurring principally in Serra dos Pirineus, Serra Dourada, and Chapada dos Veadeiros (Munhoz & Proença 1998). In spite of the fact that only a small number of specialist species restricted to specific habitats were encountered in the rocky outcrop cerrado areas studied here, a number of them (Wunderlichia cruelsiana, Schwartzia adamantium, Hyptis pachyphylla, Vellozia variabilis and V. tubiflora) were cited as being important in determining the structure of rocky outcrop cerrado sites in Caldas Novas-GO (Lima et al. 2010) and in Alto Paraíso de Goiás-GO (Lenza et al. 2011).

Of the 38 species cited by Ratter et al. (2003) as being widely distributed throughout the Cerrado biome, 37 were encountered in areas of rocky outcrop cerrado in Goiás State (table 2). According to Lima et al. (2010), these species can serve as sources of diaspores for cerrado sensu stricto areas on deep soils and can contribute to the recuperation of altered areas of that biome. Twenty-six species (11.87% of the total) were considered of limited regional abundance in the 10 areas of rocky outcrop cerrado surveyed by us in Goiás State (table 2). A species was considered of limited regional abundance in the present study if only one individual was encountered in only one of the areas inventoried. Among all the species recorded in rocky outcrop cerrado areas in Goiás State, nine (4.10%) were recorded in less than three (<10%) of the 376 areas of Cerrado studied by Ratter et al. (2003) throughout Brazil. Among these species, only two (Erythroxylum anguifugum and Miconia pepericarpa) were found among the species considered to be of limited regional abundance in the present study, reinforcing the importance of rocky outcrop cerrado sites in the preservation of species demonstrating low general abundance as well as those that are specialists in specific habitats.

The floristic similarities of the 10 survey areas as calculated by the Sørensen index varied from 0.18 to 0.71 (table 3). Values >0.50 (indicating high similarities between areas) (Kent & Coker 1992), were observed in 42.3% of the comparisons. Additionally, many of the values were between 0.45 and 0.50 (table 3), and therefore near the level of high similarity. Based on these results, it is possible to infer that there was considerable floristic similarity between the areas surveyed. On the other hand, all of the values generated by the Czekanowski index were low (<0.50), except between Jaraguá and Mara Rosa areas (table 3) – indicating that in spite of the apparent similarities in the species compositions among the different areas, differences in relative densities that gave them unique structural characteristics. In their studies of Cerrado areas (sensu stricto) in Chapada Pratinha, Chapada dos Veadeiros and São Francisco, Felfili et al. (2004) noted that species densities were one of the most important factors in differentiating between the different areas. According to those authors, this parameter must be taken into consideration when considering strategies designed to protect populations of native woody Cerrado species.

The greatest similarity values in the present study were seen between Jaraguá and Mara Rosa according to both indices, and between Jaraguá and Nazário by the Sørensen index. On the other hand, the areas of Alto Paraíso de Goiás and Piranhas showed the greatest mutual differences, and were not found in the similar to any of the other survey areas as judged by either of the indices used here. Considered together, the results of the floristic similarity analyses did not reveal any relationships between the regions or with the geographical distances between the 10 sites analyzed. These results corroborated with those reported by Felfili et al. (2004), which indicated that local environmental conditions largely determine floristic similarities of cerrado (sensu stricto) areas, independent of their geographical proximity.

Similarly, the groups formed by Two-Way Indicator Species Analysis (TWINSPAN) (figure 2) (e.g. Alto Paraíso de Goiás and Pirenópolis; Cristalina and Mineiros; Caldas Novas, Jaraguá, Mara Rosa and Nazário) did not correspond to any defined geographical area, while the areas separated by the analyses were geographically close, or even belonged to the same geographical region (e.g. Alto Paraíso de Goiás and Cavalcante). As such, the results generated by TWINSPAN likewise indicated the lack of regional influences (or of the geographical distances between the areas) on their species distributions. In general, the differences in population sizes were responsible for forming these groups as the species compositions were generally homogeneous among the different areas.

The results of the Mantel test (r=0.32, P=0.05) likewise indicated the lack of any relationships between geographical distances separating them and the floristic similarity values of the areas. In this case, the similarities of the environmental parameters were more important in the analyses than the geographical distances between the areas, as was also observed by Conceição et al. (2007) in four areas of open rocky field vegetation in the Chapada Diamantina (Bahia State). These authors observed that the closest sites were not the most floristically similar, indicating that other factors more relevant than distance were involved in determining species compositions.

Felfili et al. (2004) compared a number of cerrado sites growing on deep soils in the Chapada Pratinha, Chapada dos Veadeiros, and Espigão Mestre do São Francisco physiographic units, and encountered high floristic similarities between them. However, when some of the sites within these units were compared with the Alto Paraíso de Goiás and Chapada dos Veadeiros sites, only low similarities were found – leading the authors to believe that the Chapada dos Veadeiros region is physiographically highly heterogeneous, and that this heterogeneity is accentuated by the presence of superficial limestone and sandstone rock formations and an irregular landscape. Additionally, Chapada dos Veadeiros is considered a center of species endemism for the Cerrado biome (Simon & Proença 2000). These factors probably influenced the finding that there were 16 species exclusive to the Alto Paraíso de Goiás and Piranhas sites (both of which were examined in the present study). It is important to point out that the region near Piranhas has many granitic outcrops, which may have favored the establishment of these exclusive species. A number of authors have commented on the possibility that differences in environment conditions (such as edaphic and landscape qualities) could explain the low similarities seen between different areas (Felfili & Felfili 2001, Felfili & Silva Júnior 2005).

The peripheral geographical localization of the Alto Paraíso and Piranhas areas, together with their floristic similarities and their large numbers of exclusive species, make these areas important potential sites for the conservation of the woody rocky outcrop cerrados flora in Goiás State. According to Felfili (2007), the only conservation area in the region (the Chapada dos Veadeiros National Park) is not in itself sufficient to preserve the elevated richness and floristic heterogeneity found in the region. As such, we suggest the creation of new conservation areas in these two regions, especially in sites that have distinct edaphic conditions not represented in other established conservation sites.

The results of the present study indicate that the rocky outcrop cerrado vegetation of Goiás State has high floristic richness. Most of the species identified can also be found in cerrado sensu stricto sites on deep soils, and some of them are seen in forest environments, and small numbers of specialist species that inhabit specific and limited habitats. The combination of high richness, floristic uniqueness, and the small disturbance indices of rocky outcrop cerrados sites in Goiás State make them strategically valuable for the conservation of the woody vegetation of cerrado formations in the Cerrado biome.

Acknowledgments – The authors thank the Fundação Grupo Boticário de Proteção à Natureza for their financial support (Projects no 0651/20051 and 0765/20072); Capes for awarding study grants to the first and the last authors; CNPq/Procad UnB/Unemat for financing part of the collections and the data analyses; the specialists Carolyn Proença, Lúcia Helena Soares Silva, Manoel C. da Silva Júnior, and Bruno M. T. Walter for their help in identifying the botanical material; Camila Lima for her help in the figures elaboration; and the students Thiago Abreu, Vicente Arcela, Lívia Carrera, Julianna Maroccolo, Bárbara Bomfim, Watson Rodrigues, Elisa Bruziguessi, Thaís Lima, Renato Lôbo, Ayuni Mendes, and Mariângela Abreu for their participation in the field collections.

(received: March 29, 2011; accepted: May 31, 2012)

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  • Publication Dates

    • Publication in this collection
      18 Oct 2012
    • Date of issue
      2012

    History

    • Received
      09 Mar 2011
    • Accepted
      31 May 2011
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