Growth analysis of five Leguminosae native tree species from a seasonal semidecidual lowland forest in Brazil

Growth analysis of five Leguminosae native tree species from a seasonal semidecidual lowland forest in Brazil

Dendrochronologia 36 (2015) 23–32 Contents lists available at ScienceDirect Dendrochronologia journal homepage: www.elsevier.com/locate/dendro Orig...

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Dendrochronologia 36 (2015) 23–32

Contents lists available at ScienceDirect

Dendrochronologia journal homepage: www.elsevier.com/locate/dendro

Original article

Growth analysis of five Leguminosae native tree species from a seasonal semidecidual lowland forest in Brazil Monique S. Costa a,c , Karen E.B. Ferreira a , Paulo C. Botosso b , Cátia H. Callado a,c,∗ a Laboratório de Anatomia Vegetal, Departamento de Biologia Vegetal, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, Maracanã, 20550-900 Rio de Janeiro, RJ, Brazil b Empresa Brasileira de Pesquisa Agropecuária, Embrapa Florestas, Estrada da Ribeira, km 111—P.O. Box 319, 83411-000 Colombo, PR, Brazil c Programa de Pós-Graduac¸ão em Biologia Vegetal—UERJ, Brazil

a r t i c l e

i n f o

Article history: Received 20 October 2014 Received in revised form 4 August 2015 Accepted 18 August 2015 Available online 3 September 2015 Keywords: Atlantic rain forest Diametric annual increment Tropical tree age Growth rates Dendrochronology Growth rings

a b s t r a c t The Leguminosae family is one of the most representative families in the seasonal semidecidual lowland forest, and many of their species have economical and ecological importance, including for the recovery of degraded areas. However, there is still a lack of knowledge about the biology of native species for forest restoration. Tree growth dynamics features, such as increment rates, life expectancy and tree responses to environmental variations can be assessed through tree-ring studies. Therefore, this study aimed to investigate the growth features of Copaifera langsdorffii, Dalbergia nigra, Pterocarpus rohrii, Schizolobium parahyba and Senna multijuga trees in a known age experimental plantation. The study site was located in Espírito Santo State, southeastern Brazil. Stem discs were obtained for anatomical characterization of treerings. Wood samples were sectioned and processed following the usual plant anatomy techniques. For macroscopic analysis, samples were polished and analyzed under a stereoscopic microscope. All species showed distinct growth rings with annual periodicity formation. Growth rates, tree size measurements and growth trajectories were established for each species. These features varied even among trees of the same age and species growing under homogeneous conditions. It is noteworthy that growth variation was not related to the species’ ecological group. These data are important to characterize growth behavior of native species in order to subsidize species selection for recovery of degraded areas and economical purposes. © 2015 Elsevier GmbH. All rights reserved.

1. Introduction The Leguminosae family is the largest within the dicotyledons in Brazil (Giulietti et al., 2005). In the seasonal semidecidual lowland forest, trees from the Leguminosae family, together with those from the Myrtaceae and Sapotaceae families, bring together more than 30% of the species of the high plateaus and riparian areas (Rizzini and Garay, 2003). Leguminosae species have an important role for nitrogen fixation (Sprent, 2007), and they are economically important for food production, pharmaceutical use and construction (Lewis et al., 2005). The existence of annual growth rings was reported in many Leguminosae species growing in distinct regions (e.g. Stahle et al.,

∗ Corresponding author at: Laboratório de Anatomia Vegetal, Departamento de Biologia Vegetal, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, Maracana, 20550-900, Rio de Janeiro, RJ, Brazil. Fax +55 21 23340587. E-mail address: [email protected] (C.H. Callado). http://dx.doi.org/10.1016/j.dendro.2015.08.004 1125-7865/© 2015 Elsevier GmbH. All rights reserved.

1999; Fichtler et al., 2004; Lisi et al., 2008; Marcati et al., 2008; Callado and Guimarães, 2010; Brandes et al., 2011, 2015; Vasconcellos, 2012). The presence of tree-rings is a reflection of the environment in which the tree grew (Gasson et al., 2010). For tropical species, the formation of tree-rings is mainly associated to the existence of a dry season (Worbes, 1995). In northern Espírito Santo, the climate shows an annual dry season (Egler, 1951; Peixoto et al., 2008), which may favor the formation of distinct and annual growth rings in woody species. Thus, dendrochronology is usually applied to investigate the role of environmental factors on trees growth. It also provides information on the growth rates of trees and timber volume, which allow the construction of growth models to improve management practices, and help to determine the appropriate age for tree cutting in order to respect the cycles of population renewal (e.g., Eckstein et al., 1995; Worbes, 2002; Brienen and Zuidema, 2006; Schöngart et al., 2007; Schöngart, 2008).

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Fig. 1. Map of Espírito Santo state, in Brazil, showing the location of the study site, at Linhares city.

In tropical forests, one of the most important problems is the extraction of their woods, followed by plantation of exotic species, or by destination of the native areas for economical purposes. Historically, wood exploitation in Brazil began in the Atlantic Rain Forest, following a predatory model, which is nowadays relocated to the Amazon Forest (Cabral and Cesco, 2008). As a consequence, the Atlantic Rain Forest is one of the most threatened biomes in the world, due to a vast story of deforestation and degradation (Dean, 1995; Myers et al., 2000). Currently, only 15% of the original Atlantic Rain Forest is left (Fundac¸ão SOS Mata Atlântica/INPE, 2014). Seasonal semidecidual lowland forests of northern Espírito Santo State have undergone to exploitation of forest products and the expansion of agricultural areas, and now, they are restricted to the Sooretama Biological Reserve and the Vale Natural Reserve (Peixoto et al., 2008). These reserves are surrounded by agricul-

tural areas; alien tree plantations (mainly Eucalyptus L’Her.); and to a lesser extent, pastureland (Peixoto et al., 2008). Recently, there is an increasing effort to enable the implementation of projects to restore degraded areas next to forest remnants. Our study is inserted in Biomas Project, a Brazilian project which is concerned with the insertion of native tree species in agroforestry plantations, forest restoration and rehabilitation projects of degraded lands and forest areas. However, there is still a lack of knowledge about growth, ecology and economical use of native species. In the Atlantic Rain Forest, native tree species growing in known age plantations are relatively scarce. Investigations about these planted trees can provide valuable information on tree-rings periodicity and species’ growth rates. These data are important for implementing agroforestry plantations and degraded lands

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Table 1 Silvicultural conditions of the studied species in the experimental plantation (spacing among trees and tree age at the time of sampling); and their ecological group in the forest reserve. Species

Spacing between trees

Stand age (years)

Ecological group

C. langsdorffii D. nigra P. rohrii S. multijuga S. parahyba

3.0 × 2.5 m 2.0 × 2.0 m 2.0 × 2.0 m 2.0 × 2.0 m 2.0 × 2.0 m

30 29 22 22 22

Early secondary (1;3) Early secondary (2) Early secondary (1;2;3) Pioneer (3) Pioneer (1;3)

1. Rolim et al. (1999); 2. Rolim and Chiarello (2004); 3. Klippel (2011). Fig. 2. Climatic diagram of the study site for the period from 1986 to 2012 (data source: Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural—INCAPER).

restoration, which represent a path for the sustainable use of natural resources. Therefore, this study investigated the growth rings of five tree species growing in an experimental plantation in the seasonal semidecidual lowland forest in order to address the following questions: (1) Do species have distinct and annual tree-rings in the study site? (2) Are growth trajectories and growth rates similar among trees in plantation conditions? (3) According to the species growth rates, what is the time period required for economical use?

2. Materials and methods 2.1. Study site This study was conducted in an experimental plantation (approximately 19◦ 09 23 S, 40◦ 04 37 W) at Vale Natural Reserve (RNV), which is located about 30 km north of the city of Linhares, Espírito Santo State, southeastern Brazil (Fig. 1), with an elevation of 28–65 m above sea level (Rolim et al., 2005). The reserve is about 22.00 ha in size and it is part of one of the most important and largest remaining areas of a type of seasonal semidecidual lowland forest known as “Tabuleiro Forests” (Germano-Filho et al., 2000). This phytophysiognomy is distributed over large, flat areas, topographically characterized by vast plateaus on Tertiary deposits of crystalline rock of the Barreiras Group (Peixoto et al., 1995; Bôas et al., 2001; Garay, 2003; SEMA/UFV, 2008). In seasonal semidecidual lowland forests, about 30% of the woody species lose their leaves in the dry season (Engel, 2006). Rainfall and temperature data from the region were obtained from meteorological stations of the Instituto Capixaba de Pesquisa, Assistência Técnica e Extensão Rural—INCAPER (19◦ 06 50 S, 40◦ 04 44 W in Sooretama city and 19◦ 06 36 S, 40◦ 04 48 W in Linhares city, respectively). These climatic data covered a period of 26 years, from 1986 to 2012 and were used to calculate historical means of rainfall and temperature (Fig. 2). The climate is considered as Aw (tropical with dry winter) in the Köppen Climate Classification, with average annual rainfall of 1,200 mm. The drier and colder season occurs from May to September (mean monthly temperature from 20 to 22 ◦ C and mean monthly rainfall from 42 to 53 mm), while the wetter, and warmer season occurs from October to April (mean monthly temperature from 23 to 26 ◦ C and mean monthly rainfall from 70 to 242 mm). We evaluated the silvicultural behavior of the tree species in pure plantations under full sunlight conditions. Seedlings from the same species were all planted in the same year. Stands were planted in order to assess growth features of species with economic utilization.

2.2. Studied tree species The species selected for this study are native and belong to the Leguminosae family. Tree species from the plantation area were selected because of their occurrence also in the natural forest adjacent to the plantation. The species were classified according to their ecological groups in pioneer, early secondary or late secondary species, following the definition of Gandolfi et al. (1995). Characterization of the plantation area is presented in Table 1. The studied tree species are noted for because of their economic use and/or for their application in the recovery of degraded areas: Copaifera langsdorffii (Desf) (Caesalpinoideae), popularly known as óleo-de-copaíba, is a deciduous to semi-deciduous tree (Paula and Alves, 1997), with maximum height of approximately 15 m and diameter at breast height (DBH) up to 80 cm (Lorenzi, 2002). The species is distributed from northern to southern Brazil, and is commonly found in primary and secondary forests (Paula and Alves, 1997; Lorenzi, 2002). In the study area, the species is classified as early secondary (Rolim et al., 1999; Klippel, 2011). It provides oil with therapeutic properties (Costa-Machado et al., 2013), and it is also used in construction, furniture and tools. It is indicated for urban forestation and recovery of degraded areas (Lorenzi, 2002; Pieri et al., 2009). Dalbergia nigra (Vell.) Allemão ex Benth. (Papilionoideae), popularly known as jacarandá-da-bahia, is a deciduous tree with maximum height of approximately 25 m and DBH up to 80 cm (Paula and Alves, 1997; Lorenzi, 2002). The species is distributed from southeastern Brazil to Central America, and it is commonly found in primary and secondary forests (Lorenzi, 2002). In the study area, the species is classified as early secondary (Rolim and Chiarello, 2004). It is used in the manufacture of furniture and musical instruments, construction, urban forestation and recovery of degraded areas (Lorenzi, 2002). Pterocarpus rohrii Vahl (Papilionoideae), popularly known as pau-sangue, is an evergreen tree with maximum height of approximately 32 m, and DBH up to 100 cm (Carvalho, 2008). In the study area, this species shows deciduous behavior (personal observation), and it is classified as early secondary (Rolim et al., 1999; Rolim and Chiarello, 2004; Klippel, 2011). It is distributed from southern Brazil to Central America it is commonly found in primary and secondary forests; it is used for doors, panels, plywood, crates and charcoal production, as well as urban forestation and the recovery of degraded areas (Carvalho, 2008). Schizolobium parahyba (Vell.) S.F. Blake (Caesalpinoideae), popularly known as guapuruvu, is a deciduous tree with maximum height of approximately 30 m and DBH up to 80 cm (Paula and Alves, 1997; Lorenzi, 2002). It is distributed from southern Brazil to Mexico, and it is commonly found in open forest and secondary forest areas (Lorenzi, 2002). It is a regularly fast-growing species with a low wood specific gravity naturally occurring in the lowland and slope areas of the Atlantic Rain Forest (Shimamoto et al., 2014). In the study area, the species is classified as pioneer (Rolim et al., 1999; Klippel, 2011). It is used as core for panels and doors, to make

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Table 2 Statistics for the tree-ring chronology of each species. Species

Series intercorrelation

Spline length (years)

Average mean sensitivity

Period of chronologies (years)

Number of trees

Number of series

Mean ring width (mm)

Standard deviation

C. langsdorffii D. nigra P. rohrii S. multijuga S. parahyba

0.49 0.44 0.42 0.56 0.51

7 20 15 6 20

0.47 0.41 0.53 0.45 0.64

30 29 22 22 22

7 6 7 7 7

14 12 14 14 14

4.7 4.0 4.8 4.5 4.3

3.1 2.1 2.2 2.2 3.8

Fig. 3. Tree-ring features of Copaifera langsdorffii (A), Dalbergia nigra (B), Pterocarpus rohrii (C), Senna multijuga (D), and Schizolobium parahyba (E) viewed in transverse sections. Bar = 200 ␮m. The arrows indicate tree-rings boundaries.

shoes, crates and canoes, as well as the reforestation of degraded areas (Lorenzi, 2002; Callado and Guimarães, 2010). Senna multijuga (Rich.) H.S. Irwin & Barneby (Caesalpinoideae), popularly known as canafístula or angico-branco, is a deciduous to semi-deciduous tree, 2–10 m tall, and DBH up to 40 cm (Lorenzi, 2002; Rodrigues et al., 2005; Cardoso et al., 2012). It is a fast growing species, commonly found on the hillsides of the Atlantic Forest, and it is distributed throughout Central and South America (Lorenzi, 2002; Shimamoto et al., 2014). In the study area, the species is classified as pioneer (Klippel, 2011). It is used for crates, firewood and coal, besides being suitable for urban forestation and recovery of degraded areas (Lorenzi, 2002). 2.3. Field sampling and laboratory analysis Fieldwork was carried out in October 2011. Seven trees of each species were selected for this study, with the exception of D. nigra, which had six selected trees. Stem discs were obtained with a chainsaw, at breast height (1.30 m above ground level).

Fig. 4. Mean diametric annual increment at an age of 22 years of Copaifera langsdorffii (CL), Dalbergia nigra (DN), Pterocarpus rohrii (PR), Senna multijuga (SM) and Schizolobium parahyba (SP) trees.

2.4. Tree-rings distinctiveness In order to characterize the anatomical features of growth rings, wood samples were prepared. For microscopic analysis, the samples were transversally sectioned in a sliding microtome Leica SM 2010 R, and histological sections were stained with Safranin and

Astra Blue (Johansen, 1940; Sass, 1958; Burger and Richter, 1991). For S. parahyba histological analysis, samples were embedded in glycol methacrylate resin (Feder and O’Brien, 1968). The material was sectioned in a rotary microtome Leica RM 2025, and histological sections were stained with Toluidine Blue O (O’Brien et al.,

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Fig. 5. DBH and height of Copaifera langsdorffii (CL), Dalbergia nigra (DN), Pterocarpus rohrii (PR), Senna multijuga (SM) and Schizolobium parahyba (SP) trees.

1964). Slides were mounted with synthetic resin and then analyzed with an Olympus BX41-BF-I-20 microscope. The images of histological sections were obtained with a Q Color R3 video camera and Image-Pro Express 6.0 software. For macroscopic analysis, stem discs were polished with sandpaper of decreasing grain size (Worbes, 1995; Roig, 2000). The material was examined under a stereomicroscope for demarcation of growth layers.

the growth trajectories, we calculated moving averages using the diametric annual increment of five years’ time spans. A paired t-test was used to analyze if mean diametric annual increment differs in the transition of each five years’ time span to the next one (Zar, 1999).

2.5. Periodicity of tree-rings formation

Total height and circumference of trees at DBH were measured with a measuring tape. Total volume of each tree was calculated by the basal area multiplied by the corresponding tree height and by a form quocient, in order to consider the decrease in diameter along the stem. To calculate the form quocient, we followed Schiffel (1899), which is obtained by dividing the diameter correspondent to half of the tree height by DBH (Soares et al., 2006).

Two radii were established and measured on each stem disc. Since trees were obtained from known age experimental plantations, the growth layers were counted in order to determine periodicity of tree-ring formation. The samples were scanned, and tree-ring widths were measured with Image-Pro Plus 4.0 software. Crossdating procedures were used to check tree-rings dating (Stokes and Smiley, 1968; Speer, 2010). For assessment, measurement control and crossdating among radii of the same species, COFECHA software was used (Holmes, 1983; GrissinoMayer, 2001). With this software, it is possible to select the rigidity of the spline curve used for removing the low-frequency trend of the series (Grissino-Mayer, 2001). We tested cubic splines with different flexibility, from 5 years to 25 years, to the ring series of each species, and the spline rigidity that yielded the highest interseries correlations was used for the standardization of the tree-ring series of a certain species (Brienen and Zuidema, 2005). Based on the extension of time series, segments examined had 20 years lagged successively by 10 years. 2.6. Growth rates Based on tree-rings measurements, we calculated the cumulative radial increment for each species, by adding the measure of each ring with the measures of the previous rings. Thus, we calculated the radial annual increment by dividing the cumulative radial increment by the number of tree-rings of each tree. Then, the diametric annual increment (DAI) was calculated by multiplying the value of radial annual increment by two. Based on DAI, we calculated the estimated time span needed for each species to reach minimum logging diameter (MLD) of 50 cm, determined by the Federal Environmental Agency (IBAMA Normative Instruction number 5, December 11, 2006). To compare mean DAI of species with distinct ages, we used data corresponding to 22 years of age, the minimum age of all studied trees. Based on the cumulative radial increment, we built growth trajectory curves for each species. In order to visualize changes along

2.7. Tree size measurements

3. Results 3.1. Tree-rings distinctiveness All studied tree species presented distinct growth rings, with boundaries marked by one or more anatomical features. C. langsdorffii has distinct growth rings, marked by thickening of fiber walls in latewood and by marginal parenchyma band. The presence of secretor canals often coincides with the growth ring boundaries (Fig. 3A). D. nigra has distinct growth rings, marked by thickening of fiber walls and semi-ring porosity in association with marginal parenchyma band (Fig. 3B). P. rohrii has distinct growth rings, marked by thickening and radial flattening of fiber walls in latewood in association with semi-ring porosity and marginal parenchyma band (Fig. 3C). S. multijuga has distinct growth rings, marked by thickening and radial flattening of fiber walls in latewood, combined with marginal parenchyma band (Fig. 3D). S. parahyba has distinct growth rings, marked by marginal parenchyma band, thickening of fiber walls, and semi-ring porosity (Fig. 3E).

3.2. Periodicity of tree-rings formation Since the number of growth rings corresponded to stand age, annual periodicity of tree-ring formation was determined for all tree species in the study site. The significant correlations among tree-ring width series of each species (Table 2) also evidence the annual tree-ring formation.

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Table 3 Growth features of each species (DAI: mean Diametric Annual Increment until the age of 22 years ± standard deviation; DBH: diameter at breast height; Height; Volume and Time span to reach MLD: estimated time span needed to reach the minimum logging diameter of 50 cm). Species

DAI (mm)

DBH (cm)

Height(m)

Volume (m3 )

Time span to reach MLD(years)

C. langsdorffii D. nigra P. rohrii S. multijuga S. parahyba

10.0 (±3.0) 8.1 (±1.8) 9.8 (±2.7) 9.0 (±1.8) 8.7 (±2.0)

15.9–26.8 14.5–30.7 12.3–27.7 11.2–22.5 12.9–23.3

11.0–16.2 12.7–18.0 12.6–16.5 8.2–20.3 7.0–13.7

0.18– 0.52 0.13–0.92 0.13–0.91 0.06–0.65 0.09–0.36

51 61 51 55 57

For DBH, height and volume, the values correspond to the minimum and maximum of each species.

Fig. 6. Tree volume of Copaifera langsdorffii (CL), Dalbergia nigra (DN), Pterocarpus rohrii (PR), Senna multijuga (SM) and Schizolobium parahyba (SP) trees.

years) to IV (16–20 years) and also from time span V (21–25 years) to VI (26–29 years). P. rohrii showed high initial growth rates, which further increased until the time span from four to eight years of age; thereafter, growth rates started to decrease (Fig. 8). Growth rates decreased until the time span from 11 to 15 years of age, and after this period, little variation was observed (Fig. 8). In accordance with these changes in the growth rates, we found (Table 4) that mean DAI only differed from time span II (6–10 years) to III (11–15 years). S. multijuga showed low growth rates from one to five years of age, and then, a rising growth occurred (Fig. 8). From five to nine years of age onwards, growth rates had oscillations, but they did not show any marked period of increase or decrease (Fig. 8). Accordingly to this growth trajectory, we found (Table 4) that mean DAI only differed from time span I (1–5 years) to II (6–10 years). S. parahyba showed a prominent initial growth, with higher growth rates until the time span from four to eight years of age; thereafter, growth rates showed a decrease (Fig. 8). From six to 10 years of age onwards, growth rates showed low variations (Fig. 8). In accordance to this behavior, we found (Table 4) that mean DAI only differed from time span I (1–5 years) to II (6–10 years).

3.3. Growth rates and tree size measurements Although trees of the same species had the same age, their mean DAI, DBH, height and volume varied among trees of the same species (Table 3; Figs 4–6). These growth features also varied with different intensities for each species. The estimated time span needed to reach MLD was higher than 50 years for all the studied species (Table 3). Regarding growth trajectories, we observed differences among the studied species (Fig. 7). C. langsdorffii showed little variation during the first growth years. However, it started to show higher growth rates from seven to 11 years of age, which started to decrease from 12 to 16 years of age (Fig. 8). In the subsequent years, the trees showed growth oscillations, but they did not show any remarkable period of increase or decrease (Fig. 8). Accordingly to this behavior, we found (Table 4) that mean DAI differed from time span III (11–15 years) to IV (16–20 years). D. nigra showed little variation in growth until about 15 years of age (Fig. 8). Growth rates started to increase from 16 to 20 years of age, and began to decrease from 20 to 24 years of age onwards (Fig. 8). In accordance with this growth trajectory, we found (Table 4) that mean DAI differed from time span III (11–15

4. Discussion The distinctiveness of growth rings, as well as the correspondence among the number of rings and tree age, confirm the potential for dendrochronological investigations of the studied species in the study site. This result allowed the investigation of these species’ growth rates. The correspondence among the number of tree-rings and the plantation age showed that most of the trees reached 1.30 m high during the first plantation year. This finding is in accordance with the growth behavior of the studied species seedlings. At investigations about initial height growth in plantation conditions, C. langsdorffi showed 0.8 to 1.9 min the first year (Guedes et al., 2011; Souza, 2008; Venturoli et al., 2013; Moraes et al., 2013); D. nigra showed 1.1–3.1 m in the first year (Galvão et al., 1979; Marques et al., 2006; Gonc¸alves, 2012; Moraes et al., 2013; Pacheco et al., 2013); P. rohrii showed 0.7–3.3 m in the first year (Carvalho, 2008; Barros, 2012); S. parahyba showed 1.9–3.0 m in the first year (Souza, 2009; Nascimento et al., 2012) and S. multijuga showed 1.6–1.8 m in the first year (Lorenzi, 2002; Ferreira et al., 2007).

Table 4 Results of the paired t-test for DAI among five years’ time spans transitions. I = time span from 1 to 5 years; II = time span from 6 to 10 years; III = time span from 11 to 15 years; IV = time span from 16 to 20 years; V = time span from 21 to 25 years; VI = time span from 26 to 30 years. Time spans transitions

t values C. langsdorffii

I to II (1–5 to 6–10) II to III (6–10 to 11–15) III to IV (11–15 to 16–20) IV to V (16–20 to 21–25) V to VI (21–25 to 26–30) *

p < 0,05.

2,19 6,46 7,52* 2,68 3,87

D. nigra 0,64 1,42 3,25* 0,62 4,46*

P. rohrii 0,13 3,63* 1,65 – –

S. multijuga *

3,28 1,23 1,71 – –

S.parahyba 7,65* 0,42 0,70 – –

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Fig. 7. Cumulative radial increments of Copaifera langsdorffii, Dalbergia nigra, Pterocarpus rohrii, Senna multijuga and Schizolobium parahyba trees. Thin lines = individual growth curves; hatched line = mean curve.

Fig. 8. Moving averages of Copaifera langsdorffii, Dalbergia nigra, Pterocarpus rohrii, Senna multijuga and Schizolobium parahyba trees, for time spans of five years. Thin lines = individual growth curves; hatched line = mean curve.

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Although the intercorrelation values of most species in our study are lower than the critical value of COFECHA (0.5155; 99% of confidence level), they correspond to expected values for tropical trees, when compared with intercorrelation values obtained from other studies in South American tropics (e.g., Dünisch et al., 2003; Brienen and Zuidema, 2005; Oliveira et al., 2009; Soliz-Gamboa et al., 2011; Brandes et al., 2011). The anatomical features of C. langsdorffii, P. rohrii, S. parahyba tree-rings corresponded to the findings of different studies conducted in tropical ecosystems (Tomazello-Filho et al., 2004; Barros et al., 2008; Callado and Guimarães, 2010; Marcati et al., 2001, 2008; Lisi et al., 2008). For D. nigra, tree-ring marking by marginal parenchyma bands was previously described by Mainieri and Chimelo (1989), and different studies also reported the presence of distinct tree-rings for the species (Alves and Angyalossy-Alfonso, 2000; Gasson et al., 2010). For S. multijuga, the presence of distinct tree-rings was also observed by Shimamoto et al. (2014). The differences found in DBH in trees of the same species, with the same age, and growing under the same conditions indicate that diameter is not an appropriate parameter for age estimates of the studied species. Studies performed by Costa (2011) and Vasconcellos (2012) in the Atlantic Rain Forest with Cedrela odorata and Centrolobium robustum, respectively, have also shown no relationship between tree age and diameter. The same result was observed in C. odorata trees growing in the Bolivian Amazon where understory trees with DBH of 10 cm presented the same age as canopy trees with DBH of 60 cm (Brienen and Zuidema, 2006). Shimamoto et al. (2014) observed similar results for six species growing in a forest reserve at Brazilian southern Atlantic Rain Forest; however, they reported a positive correlation among tree age and DBH for S. parahyba and S. multijuga. This suggests that this relationship can vary according to the species growth site. According to Silva et al. (2002), tropical trees usually present different growth behavior under different conditions, even for the same species. The variation among mean DAI, DBH, height and volume of trees from the same species indicates heterogeneity in tree growth, even under homogeneous conditions. In the study reported by Bauch and Dünisch (2000), same-aged trees of Carapa guianensis (4-year-old) also showed differences in DBH (8.8–10.8 cm) and height (4.6–7.0 m). In the study conducted by Worbes (1999), sameaged trees of Cedrela odorata (about 22 years old), Tectona grandis (about 22 years old) and Sapium styllare (about 21 years old) also showed differences in DBH (28–54 cm; 16–32 cm; and 25–65 cm, respectively) and height (24–31 m; 20–22 m; and 18–30 m, respectively). Thus, growth heterogeneity within tree species seems to be a common feature in plantation tropical areas. In our study site, where spacing among trees was regular, endogenous factors (e.g. genetic structure and variability among seedlings within the species), distinct herbivory and competition pressures, or microhabitat conditions may be associated to the observed growth differences. Although S. multijuga and S. parahyba were pioneer species, only the latter showed prominent growth during the first years. In the same way, although C. langsdorffii, D. nigra and P. rohrii are early secondary species, they showed distinct growth trajectories. The mean DAI of these species also showed no clear pattern associated with their ecological groups: the early secondary species C. langsdorffii and P. rohrii showed higher growth rates than S. multijuga and S. parahyba, which are pioneer species. Only the early secondary species D. nigra showed lower growth rates than the pioneer species. The high rates of C. langsdorffii are probably related to higher spacing among trees of its stand, thereby reducing light competition. In tropical regions, the association among rainfall seasonality and tree growth is reported in distinct studies (e.g., Worbes, 1995,

1999; Priya and Bhat, 1998; Rao and Rajput, 2001; Dünisch et al., 2002; 2003; Marcati et al., 2006, 2008; Lisi et al., 2008; Brandes et al., 2015). Another study points out that growth period of a tropical species can change following local seasonality of its different growth sites (Costa et al., 2013). Concerning the mean DAI, growth rates found in the present study were distinct from other studies conducted in the Atlantic Rain Forest. These differences can be related to rainfall levels of each study site. For example, in Ilha Grande, southeastern Brazil, where annual rainfall is higher than 2000 mm, S. parahyba showed mean DAI of 22.2 mm/year (Callado and Guimarães, 2010), higher than that found in our study site. In Antonina, southern Brazil, where annual rainfall is higher than 3000 mm, S. multijuga showed DAI from 11.6 to 12.2 mm/year (Cardoso et al., 2012), also higher rates than that found in our study site. In São Paulo, southeastern Brazil, where annual rainfall is similar to our study site, but mean rainfall in the dry season is 30 mm (35% lower than our study site), S. parahyba showed mean DAI of 6.2 mm/year and C. langsdorffii, of 3.2 mm/year (Lisi et al., 2008), both lower than those found in our study site. In our studied species, the estimative of the time span needed to reach the MLD was higher than 50 years. These growth data are important to indicate native species that can be used both for the recovery of degraded areas and for economical purposes. This new economic path for agricultural producers could contribute to reduce the devastation of remnant forests. 5. Conclusion All the studied species have distinct and annual tree-rings which showed the dendrochronological potential of woody species in seasonal semidecidual lowland forest. Nevertheless, the growth trajectories and growth rates are not similar among the trees of each studied species, in spite of the same plantation conditions. Increment heterogeneity within trees of the same species suggests the influence of endogenous factors on tree growth. The variation in growth rates between the species was not related to their ecological group. The analysis of growth rates demonstrated that studied species may take from 51 to 61 years to reach to minimum diameter of 50 cm at DBH, which is the minimum diameter required by Brazilian Environmental Agency for economical use in natural areas. Thus, knowledge about native species’ growth becomes useful to recover degraded areas and to substitute the economic model which resulted in the Atlantic Rain Forest devastation. Regarding the variability of long-lived species, these results represent additional gains for trees selection strategies in future tropical tree breeding programs. Acknowledgements We thank Universidade do Estado do Rio de Janeiro (UERJ), Fundac¸ão Carlos Chagas Filho de Amparo à Pesquisa do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenac¸ão de Aperfeic¸oamento de Pessoal de Nível Superior (CAPES) - Brazil for fellowships, funding and research grants; Confederac¸ão da Agricultura e Pecuária do Brasil (CNA); EMBRAPA-Forestry and Reserva Natural Vale (RNV) for technical and financial assistance; Gilberto Terra, Jonacir Souza, Geovane Siqueira, Walter da Silva, Carlos Alberto de Oliveira and Marcos Leal Costa for support in field work; Laís dos Santos for support in samples processing; Thaís Jorge de Vasconcellos for support with artwork; Alexandre Uhlmann for helpful suggestions; and the journal reviewers for their valuable comments and suggestions on the manuscript. This paper was derived from the thesis of the first author, at PGBV/UERJ.

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References Barros, C.F., Callado, C.H., Da Cunha, M., Ferreira, M.L.M., Tamaio, N., Marquete, O., Costa, C.G., 2008. Madeiras da Mata Atlântica, 3. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, 103 pp. Barros, W.C., 2012. Avaliac¸ão do desenvolvimento de quatro espécies utilizadas na arborizac¸ão urbana no município do Rio de Janeiro. Dissertation. Universidade Federal Rural do Rio de Janeiro. Alves, E.S., Angyalossy-Alfonso, V., 2000. Ecological trends in the wood anatomy of some brazilian species. 1. Growth rings and vessels. IAWA J. 21 (1), 3–30. Bauch, J., Dünisch, O., 2000. Comparison of growth dynamics and wood characteristics of plantation-grown and primary forest Carapa guianensis in Central Amazonia. IAWA J. 21 (3), 321–333. Bôas, G.S., Sampaio, F.J., Pereira, A.M., 2001. The barreiras group in the northeastern coast of the State of Bahia, Brazil: depositional mechanisms and processes. Anais da Academia Brasileira de Ciências 73, 417–427. Brandes, A.F.N., Lisi, C.S., Barros, C.F., 2011. Dendrochronology of lianas of the Leguminosae family from the Atlantic Forest, Brazil. Trees 25, 133–144. Brandes, A.F.N., Lisi, C.S., Silva, L.D.S.A.B., Rajput, K.S., Barros, C.F., 2015. Seasonal cambial activity and wood formation in trees and lianas of Leguminosae growing in the Atlantic forest: a comparative study. Botany 93, 211–220. Brienen, R.J.W., Zuidema, P.A., 2005. Relating tree growth to rainfall in Bolivian rain forests: a test for six species using tree ring analysis. Oecologia 146 (1), 1–12. Brienen, R.J.W., Zuidema, P.A., 2006. Lifetime growth patterns and ages of Bolivian rain forest trees obtained by tree ring analysis. J. Ecol. 94, 481–493. Burger, L.M., Richter, H.G., 1991. Anatomia da Madeira. Nobel, São Paulo, 154 pp. Cabral, D.C., Cesco, S., 2008. Notas para uma história da explorac¸ão madeireira na Mata Atlântica do Sul-Sudeste. Ambiente e Sociedade 11 (1), 33–48. Callado, C.H., Guimarães, R.C., 2010. Estudo dos anéis de crescimento de Schizolobium parahyba (Leguminosae: Caesalpinioideae) após episódio de mortalidade em Ilha Grande, 33. Revista Brasileira de Botânica, Rio de Janeiro, pp. 85–91, 1. Cardoso, F.C.G., Marques, R., Botosso, P.C., Marques, M.C.M., 2012. Stem growth and phenology of two tropical trees in contrasting soil conditions. Plant Soil 354, 269–281. Carvalho, P.E.R., 2008. Espécies Arbóreas Brasileiras, 3. EMBRAPA, Brasília, 593 pp. Costa, M.S., 2011. Dinâmica de crescimento de Cedrela odorata L. (Meliaceae) na Floresta Atlântica do estado do Rio de Janeiro: fenologia, atividade cambial e dendrocronologia. In: Dissertation. Universidade do Estado do Rio de Janeiro. Costa, M.S., Vasconcellos, T.J., Barros, C.F., Callado, C.H., 2013. Does growth rhythm of a widespread species change in distinct growth sites? IAWA J. 34, 498–509. Costa-Machado, A.R.M., Bastos, J.K., Freitas, L.A.P., 2013. Dynamic maceration of Copaifera langsdorffii leaves: a technological study using fractional factorial design. Braz. J. Pharmacogn. 23 (1), 79–85. Dean, W., 1995. With Broadax and Firebrand—The Destruction of the Brazilian Atlantic Forest. University of California Press, Berkeley. Dünisch, O., Bauch, J., Gasparotto, L., 2002. Formation of increment zones and intraannual growth dynamics in the xylem of Swietenia macrophylla, Carapa guianensis, and Cedrela odorata (Meliaceae). IAWA J. 23, 101–119. Dünisch, O., Ribeiro, V., Montóia, R., Bauch, J., 2003. Dendroecological investigations on Swietenia macrophylla King and Cedrela odorata L. (Meliaceae) in the central Amazon. Trees 17, 244–250. Eckstein, D., Sass, U., Baas, P., 1995. Preface. IAWA J. 16 (4), pp.325. Egler, W.A., 1951. A zona pioneira ao Norte do Rio Doce. Revista Brasileira de Geografia, ano 13, n.2, 223–264. Engel, V.L., 2006. Estudo Fenológico De Espécies Arbóreas De Uma Floresta Tropical Em Linhares —es. Phd Thesis. UNICAMP) Campinas University. Feder, N., O’Brien, T.P., 1968. Plant microtechnique: some principles and new methods. Am. J. Bot. 55, 123–142. Ferreira, R.A., Davide, A.C., Bearzoti, E., Motta, M.S., 2007. Semeadura direta com espécies arbóreas para recuperac¸ão de ecossistemas florestais. Cerne 13 (3), 271–279. Fichtler, E., Trouet, V., Beeckman, H., Coppin, P., Worbes, M., 2004. Climatic signals in tree rings of Burkea africana and Pterocarpus angolensis from semiarid forests in Namibia. Trees 18, 442–451. Fundac¸ão SOS Mata Atlântica/INPE, Atlas Dos Remanescentes Florestais Da Mata Atlântica—Período, 2012–2013, 2014, Relatório Técnico, São Paulo, 61pp. Galvão, A.P.M., Ferreira, C.A., Teixeira, L.B., 1979. Observac¸ões sobre o comportamento do jacarandá-da-bahia (Dalbergia nigra Fr. Allem.) em povoamento puro na Amazônia, 19. IPEF, pp. 47–59. Gandolfi, S., Leitão-Filho, H.F., Bezerra, C.L.F., 1995. Levantamento florístico e caráter successional das espécies arbustivo-arbóreas de uma floresta mesófila semidecídua no município de Guarulhos, SP. Rev. Bras. Biol. 55 (4), 753–767. Gasson, P., Miller, R., Stekel, D.J., Whinder, F., Ziemin´ıska, K., 2010. Wood identification of Dalbergia nigra (CITES Appendix I) using quantitative wood anatomy, principal components analysis and naïve Bayes classification. Ann. Bot. 105, 45–56. Garay, I., 2003. A dimensão funcional da diversidade biológica, in: Garay, I., Rizzini, C.M. A Floresta Atlântica de Tabuleiros—Diversidade funcional da cobertura arbórea. Vozes, Petrópolis, pp. 50–53. Germano-Filho P., Peixoto A. L., Jesus R. M., 2000. Espécies vegetais descritas a partir de espécimes coletados na Reserva Florestal de Linhares, Espirito Santo, Brasil. Boletim do Museu de Biologia. Mello Leitão (N. Ser.) 11/12: 35–48. Giulietti, A.M., Harley, R.M., Queiroz, L.P., Wanderley, M.G.L., Van den Berg, C., 2005. Biodiversidade e conservac¸ão das plantas no Brasil. Megadiversidade 1 (1), 52–61.

31

Gonc¸alves, I.F.S., 2012. Resposta De Três Espécies Nativas De Mata Atlântica a Diferentes Condic¸ões De Luminosidade Dissertation. Universidade Federal Rural do Rio de Janeiro. Grissino-Mayer, H.D., 2001. Evaluating crossdating accuracy: a manual and tutorial for the computer program COFECHA. Tree-Ring Res. 57 (2), 205–221. Guedes, M.G.M., Silva-Júnior, M.L., Silva, G.R., Silva, A.L.P., Lima-Junior, J.A., 2011. Desenvolvimento inicial e composic¸ão mineral de copaíba cultivadas em latossolo amarelo, textura média, sob omissão de nutrientes. Enciclopédia Biosfera, Centro Científico Conhecer, Goiânia, vol.7, n.12, pp. 1-13. Holmes, L.R., 1983. Computer assisted quality control in tree-ring dating and measurement. Tree-ring Bull. 43, 69–78. Johansen, D.A., 1940. Plant Microtechnique. McGraw-Hill, New York. Klippel, V.H., 2011. Avaliac¸ão de métodos de restaurac¸ão florestal de Mata Atlântica de Tabuleiros. Dissertation. Univesidade Federal do Espírito Santo. Lisi, C.S., Tomazello-Filho, M., Botosso, P.C., Roig, F.A., Maria, V.R.B., Ferreira-Fedele, L., Voigt, A.R.A., 2008. Tree-ring formation, radial increment periodicity, and phenology of tree species from a seasonal semi-deciduous forest in Southeast Brazil. IAWA J. 29 (2), 189–207. Lewis, G.P., Schire, B., Mackinder, B., Lock, M., 2005. Legumes of the World. Royal Botanic Gardens, Kew, 577 pp. Lorenzi, H., 2002. Árvores brasileiras: manual de identificac¸ão e cultivo de plantas arbóreas do Brasil, v. 1. Plantarum, Nova Odessa, 368 pp. Mainieri, C., Chimelo, J.P., 1989. Fichas de características das Madeiras Brasileiras. Instituto de Pesquisas Tecnológicas –IPT, São Paulo, 420 pp. Marcati, C.R., Angyalossy-Alfonso, V., Benetati, L., 2001. Anatomia comparada do lenho de Copaifera langsdorffii Desf. (Leguminosae-Caesalpinoideae) de floresta e cerradão. Revista Brasileira de Botânica 24 (3), 311–320. Marcati, C.R., Angyalossy, V., Evert, R.F., 2006. Seasonal variation in wood formation of Cedrela fissilis (Meliaceae). IAWA J. 27 (2), 199–211. Marcati, C.R., Milanez, C.R.D., Machado, S.R., 2008. Seasonal development of secondary xylem and phloem in Schizolobium parahyba (Vell.) Blake (Leguminosae: Caesalpinioideae). Trees 22, 3–12. Marques, V.B., Paiva, H.N., Gomes, J.M., Neves, J.C.L., Bernardino, D.C.S., 2006. Efeito de fontes e doses de nitrogênio sobre o crescimento inicial e qualidade de mudas de jacarandá-da-bahia (Dalbergia nigra (Vell.) Fr. All. ex Benth.). Revista Árvore 30 (5), 725–735. Moraes, L.F.D., Assumpc¸ão, J.M., Pereira, T.S., Luchiari, C., 2013. Manual técnico para a restaurac¸ão de áreas degradadas no Estado do Rio de Janeiro. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro, pp84. Myers, N.R.A., Mittermeier, C.G., Mittermeier, G.A.B., Fonseca Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 852–858. Nascimento, D.F., Leles, P.S.S., Oliveira-Neto, S.N., Moreira, R.T.S., Alonso, J.M., 2012. Crescimento inicial de espécies florestais em diferentes espac¸amentos. Cerne 18 (1), 159–165. O’Brien, T.P., Feder, N., McCully, M.E., 1964. Polychromatic staining of plant cell walls by Toluidine Blue O. Protoplasma 59 (2), 368–373. Oliveira, J.M., Roig, F.A., Pillar, V.P., 2009. Climatic signals in tree-rings of Araucaria angustifolia in the southern Brazilian highlands. Aust. Ecol. 35 (2), 134–147. Pacheco, F.V., Pereira, C.R., Silva, R.L., Alvarenga, I.C.A., 2013. Crescimento inicial de Dalbergia nigra (Vell.) Allemão ex. Benth. (Fabaceae) e Chorisia speciosa A. St. -Hil (Malvaceae) sob diferentes níveis de sombreamento. Revista Árvore 37 (5), 945–953. Paula, J.E., Alves, J.L.H., 1997. Madeiras nativas: anatomia, dendrologia, dendrometria, produc¸ão, uso. Fundac¸ão Mokiti Okada, Brasília, 541 pp. Peixoto, A.L., Rosa, M.M.T., Joels, L.C.M., 1995. Diagramas de perfil e de cobertura de um trecho da Floresta de Tabuleiro na Reserva Florestal de Linhares (Espírito Santo, Brasil). Acta Botanica Brasilica 9 (2), 177–193. Peixoto, A.L., Silva, I.M., Pereira, O.J., Simonelli, M., Jesus, R.M., Rolim, S.G., 2008. Tabuleiro Forests North of the Rio Doce: Their representation in the Vale do Rio Doce Natural Reserve, 100. Memorial New York Botanical Garden, Espírito Santo, Brazil, pp. 319–350. Pieri, F.A., Mussi, M.C., Moreira, M.A.S., 2009. Óleo de copaíba (Copaifera sp.): histórico, extrac¸ão, aplicac¸ões industriais e propriedades medicinais, 11. Revista Brasileira de Plantas Medicinais, Botucatu, pp. 465–472, 4. Priya, P.B., Bhat, K.M., 1998. False ring formation in teak (Tectona grandis L. f.) and the influence of environmental factors. For. Ecol. Manag. 108, 215–222. Rao, K.S., Rajput, K.S., 2001. Relationship between seasonal cambial activity, development of xylem and phenology in Azadirachta indica growing in different forests of Gujarat State. Ann. For. Sci. 58, 691–698. Rizzini, C.M., Garay, I., 2003. A esclerofilia foliar como indicador funcional do status da biodiversidade em Floresta Atlântica de Tabuleiros. In: Garay, I., Rizzini, C.M. (Eds.), A Floresta Atlântica de Tabuleiros —Diversidade funcional da cobertura arbórea. Vozes, Petrópolis, pp. 50–53. Rodrigues, R.S., Flores, A.S., Miotto, S.T.S., Baptista, L.R.M., 2005. O gênero Senna (Leguminosae, Caesalpinioideae) no Rio Grande do Sul, 19. Acta Botanica Brasilica, Brasil, pp. 1–16. Roig, F.A., 2000. Dendrocronología en los bosques del Neotrópico: revisión y prospección futura. In: Roig, F.A. (Ed.), Dendrocronología en América Latina. EDIUNC, Mendoza, 434 pp. Rolim, S.G., Couto, H.T.Z., Jesus, R.M., 1999. Tree mortality and recruitment in the Atlantic Forest at Linhares (ES). Sci. For. 55, 49–69. Rolim, S.G., Chiarello, A.G., 2004. Slow death of Atlantic forest trees in cocoa agroforestry in southeasthern Brazil. Biodivers. Conserv. 13, 2679–2694. Rolim, S.G., Jesus, R.M., Nascimento, H.E.M., Couto, H.T.Z., Chambers, J.Q., 2005. Biomass change in an Atlantic tropical moist forest: the ENSO effect in permanent sample plots over a 22-year period. Oecologia 142, 238–246.

32

M.S. Costa et al. / Dendrochronologia 36 (2015) 23–32

Sass, J.E., 1958. Elements of Botanical Microtechnique, 2. McGraw-Hill Book Company, New York, pp.222. Schiffel, A., 1899. Form und Inhalt der Fichte. Mitt. Fortl. Versuchswes, Österreichs, 24, Wien. Schöngart, J., Wittmann, F., Worbes, M., Piedade, M.T.F., Krambecka, H.J., Junk, W.J., 2007. Management criteria for Ficus insipida Willd. (Moraceae) in Amazonian white-water floodplain forests defined by tree-ring analysis. Ann. For. Sci. 64, 657–664. Schöngart, J., 2008. Growth-Oriented Logging (GOL): A new concept towards sustainable forest management in Central Amazonian várzea floodplains. For. Ecol. Manag. 256, 46–58. SEMA, 2008. In: Vitória, E.S. (Ed.), Atlas de Ecossistemas do Espírito Santo. SEMA/UFV, Vic¸osa, 504 pp. Shimamoto, C.Y., Botosso, P.C., Marques, M.C.M., 2014. How much carbon is sequestered during the restoration of tropical forests? Estimates from tree species in the Brazilian Atlantic forest. Forest Ecol. Manag. 329, 1–9. Silva, R.P., Santos, J., Tribuzy, E.S., Chambers, J.Q., Nakamura, S., Higuchi, N., 2002. Diameter increment and growth patterns for individual tree growing in Central Amazon, Brazil. For. Ecol. Manag. 166, 295–301. Soares, C.P.B., Paula-Neto, F., Souza, A.L., 2006. Dendrometria e inventário florestal. Editora Universidade Federal de Vic¸osa, Vic¸osa, 276 pp. Soliz-Gamboa, C.C., Rozendaal, D.M.A., Ceccantini, G., Angyalossy, V., Borg, K., Zuidema, P.A., 2011. Evaluating the annual nature of juvenile rings in Bolivian tropical rainforest trees. Trees 25 (1), 17–27. Souza, M.C.S., 2009. Monitoramento de Sistemas Agroflorestais Para Recuperac¸ão de Áreas Degradadas da Floresta Ombrófila Densa: Caso Paraty — RJ. Dissertation. Centro de Ciências Agrárias, Universidade de São Carlos. Speer, J.H., 2010. Fundamentals of Tree-Ring Research. The University of Arizona Press, 324 pp.

Sprent, J.I., 2007. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol. 174, 11–25. Stahle, D.W., Mushove, P.T., Cleaveland, M.K., Roig, F., Haynes, G.A., 1999. Management implications of annual growth rings in Pterocarpus angolensis from Zimbabwe. For. Ecol. Manag. 124, 217–229. Stokes, M., Smiley, T., 1968. An Introduction to Tree-ring Dating. The University of Chicago Press, Chicago and London, 73 pp. Tomazello-Filho, M., Lisi, C.S., Hansen, N., Cury, G., 2004. Los generos de Caesalpinioideae (Leguminosae) presentes en Sudamerica. Sci. Florestalis 66, 46–55. Vasconcellos, T.J., 2012. Dinâmica de crescimento de Centrolobium robustum (Vell.) Mart. ex Benth. (Leguminosae-Papilionoideae) na Floresta Atlântica. In: Dissertation. Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brasil. Venturoli, F., Venturoli, S., Borges, J.D., Castro, D.S., Souza, D.M., Monteiro, M.M., Calil, F.N., 2013. Incremento de espécies arbóreas em plantio de recuperac¸ão de área degradada em solo de Cerrado no Distrito Federal. Biosci. J. 29 (1), 143–151. Worbes, M., 1995. How to measure growth dynamics in tropical trees—a review. IAWA J. 16 (4), 337–351. Worbes, M., 1999. Annual growth rings, rainfall-dependent growth and long-term growth patterns of tropical trees from the Caparo forest reserve in Venezuela. J. Ecol. 87, 391–403. Worbes, M., 2002. One hundred years of tree-ring research in the tropics—a brief history and an outlook to future challenges. Dendrochronologia 20 (1–2), 217–231. Zar, J.H., 1999. Biostatistical Analysis. Prentice Hall, New Jersey, pp. 663.