J. Mt. Sci. (2014) 11(4): 875-883
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http://jms.imde.ac.cn DOI: 10.1007/s11629-013-2792-4
Relationship between Physical and Chemical Soil Attributes and Plant Species Diversity in Tropical Mountain Ecosystems from Brazil
Fernanda de CARVALHO1,2*, Edward Luis GODOY3, Francy J. G. LISBOA4, Fatima Maria de Souza MOREIRA2, Francisco Adriano de SOUZA5, Ricardo Luis Louro BERBARA4, G Wilson FERNANDES1 1 Laboratory of Evolutionary Ecology and Biodiversity, Department of Geral Biology, Institute of Biology Sciences, Federal University of Minas Gerais, Belo Horizonte MG 30161-901, P.O. Box 486, Brazil 2 Department of Biology, Microbiology and Biological Processes, Department of Soil Science, Federal University of Lavras, Lavras, Minas Gerais 37200-000, P.O.Box 3037, Brazil 3 Department of Biological Sciences, Ferderal University of São João Del Rei, São João del-Rei, Minas Gerais 36307-352, Brazil 4 Laboratory of Soil Biology, Department of Soil Science, Federal Rural University of Rio de Janeiro, Seropédica, Rio de Janeiro 23890-000, Brazil 5 Embrapa Maize and Sorghum, Center for Applied Biology, Rod. MG 424 KM 45, Caixa Postal, Sete Lagoas, Minas Gerais 35701-970, P.O. Box 285, Brazil *Corresponding author, e-mail:
[email protected]; Tel.: +55313829 1225; Fax: +553538291251 Citation: de Carvalho F, Godoy EL, Lisboa FJG, et al. (2014) Relationship between physical and chemical soil attributes and plant species diversity in tropical mountain ecosystems from Brazil. Journal of Mountain Science 11(4). DOI: 10.1007/s11629013-2792-4
© Science Press and Institute of Mountain Hazards and Environment, CAS and Springer-Verlag Berlin Heidelberg 2014
Abstract: Although the high diversity of plant species in the rupestrian fields has been primarily attributed to the existence of a set of distinct habitats, few studies support this assertion. The present study aimed to further investigate the relationship between physical and chemical attributes of soils with the diversity of plant species in this unique ecosystem. The rupestrian field is a unique vegetation formation that covers some of the southeastern Brazilian mountains in the transition of the Atlantic rain forest and the Cerrado (savanna). Different habitats occur according to soil characteristics (e.g., presence of rocks, sand, fertility, hydrology, etc.). These attributes ultimately influence the vegetation that is highly adapted to the harsh edaphic and climatic mountain conditions. Five distinct habitats were studied by us: rocky outcrops, peat bogs, sandy bogs, quartz gravel Received: 29 May 2013 Accepted: 5 November 2013
fields, and “cerrado” (savanna). A floristic survey indicated that four families are found at greater frequency: Poaceae, Asteraceae, Cyperaceae, and Leguminosae. The greatest diversity of plant species was found in the rocky outcrops habitat, followed by cerrado, peat bog, quartz gravel grassland, and sandy bogs, respectively. The main difference in the floristic composition among these habitats was related to the dominant species. Trachypogon spicatus (Poaceae) was the most dominant species in the rocky outcrops, Axonopus siccus (Poaceae) in the peat bogs, Lagenocarpus rigidus (Cyperaceae) in the sandy bogs, Schizachyrium tenerum (Poaceae) in the cerrado, while Vellozia sp. 8 (Velloziaceae) dominated the vegetation in the quartz gravel grassland. This study demonstrated that physical and chemical soil properties strongly related the diversity of plant species occurring in the different habitats of rupestrian fields.
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Keywords: Floristic diversity; Plant-soil relationships; Espinhaço Range; Biodiversity; Mountain ecology; Plant habitat
Introduction
Conceição and Pirani 2005; de Carvalho et al. 2012). The extremely high diversity and high degree of endemism found in rupestrian fields have always been associated with this mosaic of habitats and their singularities. However, little is known about their soil attributes and even less about their intrinsic plant diversity. The present study aimed to investigate the physico-chemical attributes of soils and the diversity of plant species, as well as their relationships in the different habitats that constitute the mosaic of rupestrian fields.
The Espinhaço mountain range has approximately 1100 km in the NS direction and 50 to 100 km in the EW direction. The mountains span along the range 20°35' S and 11°11' S, and are bounded at the north by the Serra da Jacobina, in Juazeiro - Bahia and at the south by the Serra de Ouro Branco, in Ouro Branco, Minas Gerais, Brazil 1 Material and Methods (Derby 1906; Harley 1995). This mountain range is the natural divisor of two important areas of vegetation (Menezes and Giulietti 1986) considered The study was conducted in the Vellozia global hotspots (Myers et al. 2000) - the Atlantic Reserve (lat 19°16'45.7" S, long 43°35'27.8" W), Forest, on the eastern slope, and the “Cerrado”, on Serra do Cipó, Minas Gerais, Brazil (Figure 1) The the western slope. Above 900 m of altitude in this climate type is tropical of altitude with cool mountain range the so-called rupestrian field summers and well defined dry season between the vegetation predominates. Belonging to the Cerrado months of May and September. Average annual biome, the rupestrian fields are considered a temperatures are around 21.2°C and the average unique ecosystem, known for its diverse flora and annual rainfall is 1622 mm (Madeira and numerous endemic species (Giulietti et al. 1987). It Fernandes 1999). is estimated that in the southern part of the Cadeia To investigate the relationship between the do Espinhaço, in Serra do Cipó, in Minas Gerais physical and chemical properties of the soil and the state, more than 3000 plant species can be found, diversity of plant species in the different rupestrian and a third of them are exclusive of the region field habitats (Figure 2), we firstly delimitated the (Giulietti et al. 1997, 2000). Due to strong habitats found. The delimitation of habitats anthropogenic pressures on this ecosystem, many proceeded according to the visual characteristics of rupestrian field species are now endangered (Viana the soil, the limits of vegetation, and if habitats et al. 2005; Barbosa et al. 2010). maintained soaked or not in the rainy season (for The rupestrian field vegetation is known for details see de Carvalho et al. 2012). Five distinct its high spatial heterogeneity owing to its complex habitats were easily found in the study area: Peat mosaic of habitats that occurs side-by-side (Conceição and Giulietti 2002; Conceição and Pirani 2005, 2007; Medina and Fernandes 2007; de Carvalho et al. 2012, Negreiros et al. 2014). These habitats are visually separated by soil configuration, continuity of vegetation, floristic composition, proportion of exposed rock, and sandy sediments, among other factors. Moreover, in the rainy season the soils of some of these habitats can dry up while others remain humid (Conceição 2000; Figure 1 Location of Serra do Cipó at State of Minas Gerais (MG) Conceição and Giulietti 2002; Municipality Brazil.
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Figure 2 Habitats found in the Serra do Cipo area studied. (A) Rupestrian field mountains; (B) Peat Bogs; (C) Sandy bogs; (D) Quartz gravel fields; (E) Cerrado and (F) Rocky outcrops.
bogs – occur above 1000 m – different from a sandy bog, the peat bog remains constantly soggy during the rainy season. There is a predominance of a herbaceous stratum (Figure 2B); Sandy bogs – occur above 1000 m a.s.l. – suffers periodic water loggings in the rainy season. The herbaceous vegetation occurs continuously (Figure 2C); Quartz gravel field – occur in quotas above 1000 m – this habitat has the peculiarity of the soil surface being covered by small quartzite rock fragments (Figure 2D); cerrado (savanna) – between 800 to 1200 m a.s.l. occurs patches of cerrado, whose dominance of species in shrub-tree forms declines with increasing altitude and lower stage of development of the soil profile, gradually or abruptly becoming rupestrian fields. In this study cerrado areas are above 1000 m a.s.l., while in many instances they abruptly shifts to rupestrian fields (Figure 2E); Rocky outcrops – occur above 1000 m a.s.l. areas
with high proportions of exposed rock and herbaceous and shrubby vegetation that grow directly on top of rock or in micro-sites or thin soil layers where there are conditions for root development. They are remarkably discontinuous (Figure 2F). Once defined, the corresponding areas of each habitat were randomly selected into 3 plots of 50 m × 20 m; each of them divided into five subplots of 5 m × 5 m in order to proceed with more detailed description. Overall, we had three plots with 15 subplots (375 m2) per habitat. The geographical position and altitude of plots were described in detail in de Carvalho et al. (2012). For the study of floristic diversity, representative branches of each plant species were collected and prepared for further identification of species. Branches of the plants found within the plots were later collected for their species identification (December, 2006
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through July, 2008) due to their distinct phonological patterns. The taxonomic identifications were done with the participation of experts and visits to the herbariums at the Federal University of Minas Gerais (BHCB) and Federal University of Lavras (HESAL) plus specialized literature. The names of the families follow the classification of Cronquist (1981), except for the Leguminosae. To evaluate habitat plant species diversity we used the Shannon diversity index based on natural logarithmic, while the Pielou’s evenness (J) was used to represent the distribution uniformity of individuals of all existing species (Magurran 1988). Samples of soils were done once at each sample plot. Sampling and characteristics of soil attributes are in de Carvalho et al. (2012). We tested the null hypothesis of absence of heterogeneity, or presence of homogeneity, in the multivariate dispersion between the five habitats evaluated. Multivariate dispersion analysis is similar to Levene’s test for homogeneity of variances for univariate data, and can be used as a measure of environmental and floristic heterogeneity between different groups (Anderson et al. 2006). This analysis assesses the heterogeneity between groups based on the average distance to a measure of central tendency within each group, either a median or a centroid. Three analyses were conducted in the present study: floristic distance matrix (Hellinger distance), Euclidean distance matrix of standardized soil chemical variables (mean of zero and standard deviation equal to one) and the Euclidean distance matrix of standardized soil physical variables. The measure of central tendency used for all analyses was the median because it exhibits a more accurate Type I error rate. The significance of heterogeneity was assessed using a permutation test (10,000 randomizations) and the P- and F-values were reported. The significant results in the multivariate dispersion analysis were plotted and the environmental vectors, i.e., the variables significantly correlated (P < 0.05) with the ordination axes, were used to help with the interpretation of the results. Variance partitioning based on redundancy analysis (RDA) was conducted to access the power for three groups of data as floristic composition structure drivers: chemical, physical variables, and
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geographic distance. Prior to the analysis, plant community data were Hellinger transformed by reducing the most abundant species’ weight (Legendre and Gallagher 2001). Each soil fertility (pH, Ca, Mg, Al, P, SOM, N, Fe, Mn, and Zn) and physical variable (gravel, coarse sand, fine sand, silt, and clay) was previously standardized to reduce the weight for the different scales. UTM coordinates were used to include space in the model. Here, distance in causal models was adequate to discern the linear trends (Laliberté et al. 2009). From the UTM coordinates, we developed a second-order polynomial using the monomials to model nonlinear spatial structures, wherein the spatial information was described by Northing, Easting, Northing × Easting, Northing2, and Easting2. After transformation, the monomials were centralized but not divided by the standard deviation to maintain the relationships between the coordinates. An overall RDA (including all explanatory variables) was conducted for each of the three explanatory variable groups. The plant community was used as the response. Significance was tested to continue the variable selection process. The variables were selected according to the two criteria described by Blanchet et al. (2008). The selected variables were used for variance partitioning, and the following fractions were calculated: [a], “solely chemical variable effect”; [b], “solely physical variable effect”; [c], “solely geographical distance effect”; and [d], “unmeasured factor effect”. For the individual fractions [a], [b], and [c], significance was tested by a partial RDA. The adjusted R2 was reported for each fraction.
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Results
A total of 171 plant species were found within the five habitats that constitute the mosaic of rupestrian field. The average plant species density was 0.0912 species/m2. These species were distributed into 110 genera and 44 families. The families with high species richness were: Poaceae (31), Asteraceae (26), Cyperaceae (11), Leguminosae (11), Velloziaceae (9), Melastomataceae (9), Eriocaulaceae (8), Rubiaceae (7), Myrtaceae (5), Malpighiaceae (5) Lythraceae
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(4), and Convolvulaceae (3). These 12 families constituted 75.43% of the species, while the other 32 families constituted 24.57% of the species. Among the habitats studied, the rocky outcrops showed the largest number of species (79), followed by cerrado (65), peat bogs (55), quartz gravel field (52), and sandy bog (25). The main differences according to floristic composition between these habitats were the dominant species. Trachypogon spicatus (Poaceae) dominated in the rocky outcrops, Axonopus siccus (Poaceae) in peat bogs, Lagenocarpus rigidus (Cyperaceae) in sandy fields, Schizachyrium tenerum (Poaceae) in cerrado, while Vellozia sp. 8 was the dominant species in the quartz gravel fields. The Shannon diversity index indicated that the greatest diversity of plant species was found in the rocky outcrops (2.74 nats/individual), followed by cerrado (2.51 nats/individual), peat bog (2.02 nats/individual), quartz gravel field (1.89 nats/individual), and sandy bog (1.59 nats/individual). The Pielou’s evenness (J) presented the following order: 0.79 for cerrado, 0.71 for rocky outcrop, 0.64 for peat bog, and sandy bog, and 0.58 for quartz gravel field. The endemic woody species of Serra do Cipó Coccoloba cereifera (Polygonaceae) was found in the rocky outcrop, sandy bog, and quartz gravel field habitats. The endemic palm, Syagrus pleiocada (Arecaceae), was found primarily in rocky outcrops and cerrado habitats. The species Calliandra fasciculata (Leguminosae) was solely found in the cerrado habitat, while the rare grass species Paspalum falcatum (Poaceae) was found only in the peat bog habitat. Floristic heterogeneity was found in the multivariate dispersion analysis (Figure 3). However, a pairwise comparison of heterogeneity (Tukey’s HSD, 95%) showed that the significant dispersion of floristic data identified by the analysis occurs only due to the differences between two habitats: the cerrado and the sandy bogs (P = 0.014). This result suggests that the remaining sites represent an intermediate stage of floristic composition. The ordination using environmental vectors (soil chemical and physical variables) shows that cerrado and sandy bog habitats are the most contrasting habitats (Figure 3). However, the habitats (cerrado and sandy bog) were considered homogeneous regarding both the soil chemical (F =
0.835; P > 0.05) and physical (F = 0.166; P > 0.05) variables.
Figure 3 Ordination in the Euclidean space of the five habitats evaluated for homogeneity of multivariate dispersion around the median. Ordination based on the floristic distance matrix (Hellinger distance). The significance of the degree of heterogeneity between habitats was tested using 10,000 randomizations. The vectors represent only the environmental variables significantly correlated with the ordination axes (P < 0.05).
The overall RDA showed that the plant community composition in the sites studied was influenced by all three sets used as predictors. For the soil variables, forward variable selection generated a model with only three variables: Mn, Fe, and Al. The RDA conducted using only these three predictors showed that approximately 27% (R2adj = 0.27, P < 0.001) of the floristic variation was driven by the chemical attributes of the soil. The physical variables clay content, coarse sand content, and gravel were the three variables used after testing the significance of the overall model, which included all of the variables. The model with these three variables explained 23% of the plant community variation (Table 1). To access the non-linear spatial relationships, second-order monomials were not selected for the procedure adopted herein (forward selection, Blanchet et al. 2008). The variable selected was the first-order coordinate “Easting”. The variance partitioning between the chemical variables, physical variables, and geographical distance was based on the variables selected via the RDA and showed that fraction [c] (“solely spatial effect”) accounted for only 0.09% of the floristic composition variation; this fraction was not considered significant (Figure 4). Fractions
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all floristic surveys that included other areas of rupestrian field vegetation located in the states of Model Variables RDA axes Bahia and Minas Gerais (Andrade R2adj P R2adj P R2adj P 0.27 *** Mn 0.13 *** RDA1 0.14 *** et al. 1986; Giulietti et al. 1987; Chemical Fe 0.091 ** RDA2 0.10 *** Conceição and Giulietti 2002; Al 0.087 ** RDA3 0.07 *** Vitta 2002; Conceição and Pirani 0.23 *** Clay 0.12 *** RDA1 0.14 *** 2005, 2007; Mourão Stehmann Coarse Physical 0.086 ** RDA2 0.084 * 2007). sand Gravel 0.083 * RDA3 0.062 ns The distinctions among the dominant species in each habitat Note: We only selected one spatial variable which is not shown here (see the main text). The results are shown with adjusted R2 values. Model indicated structural differences, stands for total floristic composition variance explained by the two RDA as observed by calculations of models (Chemical and Physical). Variables column takes account for ecological indices. The estimated individual soil predictors that more explained floristic variation within each degree for evenness in the model. Finally, RDA axes column shows the variance explained by the three first axes within each RDA model Significance was investigated through habitats cerrado and rocky 10000 randomizations. ***P
