Liana community ecology and interaction with Parapiptadenia rigida (Bentham) Brenan in a fragment of secondary forest

Forest Ecology and Management 307 (2013) 84–89

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Liana community ecology and interaction with Parapiptadenia rigida (Bentham) Brenan in a fragment of secondary forest Thomas Schröder ⇑, Frederico D. Fleig, Vinicios Spadetto Universidade Federal de Santa Maria, Engenharia Florestal, Campus Universitario, 97105-900 RS, Santa Maria, Brazil

a r t i c l e

i n f o

Article history: Received 6 April 2013 Received in revised form 26 June 2013 Accepted 27 June 2013 Available online 31 July 2013 Keywords: Liana ecology Competition Tree growth Secondary forest management

a b s t r a c t The development of effective silvicultural prescriptions for Atlantic forest secondary patches could offset the amount of exploitative logging in Amazonian forests. This study described the diameter growth response of Parapiptadenia rigida (Fabaceae), a dense wooded, fast-growing canopy tree, to liana competition in attempt to determine silvicultural prescriptions for this species in natural forests. Field procedures were carried out in one fragment of natural forest, in which one hundred 0.01 ha plots and 50 individual trees of the target species were selected. We found 23 species in the liana community, which was strongly dominated by Senegalia tucumanensis (Fabaceae). P. rigida had more lianas infesting it compared to the overall forest and its presence increased the abundance of S. tucumanensis. Trees with more than 50% of the crown occupied by lianas had a lower height:diameter ratio. Liana below-ground competition, measured by liana basal area around target trees, reduced diameter increment in P. rigida. The studied species showed great potential for timber production due to fast growth, wood quality and carbon sequestration. The developed individual tree diameter growth model shows that silvicultural treatments could increase diameter growth to about 1.5 cm/year. Ó 2013 Elsevier B.V. All rights reserved.

1. Introduction The Brazilian Atlantic forest is characterized by its high biological endemism and structural diversity (Negrelle, 2002). It is a highly fragmented ecosystem with 20% of its remaining area located 50 m from a forest edge (Ribeiro et al., 2009) and most of the ecosystem is composed of secondary forests. Most of the Brazilian population occurs within the boundaries of this ecosystem and it was the primary source of energy and construction material to building the social infrastructure of the country. Currently, the majority of high quality wood in Brazil comes from Amazonian forests (Barreto, 2006). Silvicultural prescriptions for natural forests based solely on cutting cycle, harvest volume and liana cutting are unlikely to provide sustainable harvestable volume (Peña-Claros et al., 2008; Keefe et al., 2009; Villegas et al., 2009; Schwartz et al., 2013). This happens because many of these silvicultural prescriptions for tropical forests were developed in southeastern Asia (Dawkins and Philip, 1998) and may not be applicable to Neotropical forests. In order to increase ecological sustainability and harvest revenue, silvicultural treatment prescriptions that are proved to be economically and ecologically sound need to be developed for natural forest management. ⇑ Corresponding author. Tel.: +55 (55)81558844. E-mail address: [email protected] (T. Schröder). 0378-1127/$ - see front matter Ó 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.foreco.2013.06.063

Although a great deal of effort has been made for the conservation and the sustainable management of the Amazon forest, it is unlikely to be successful unless there is also the rational use of Atlantic forest (De Graaf et al., 2003). Brazilian laws (Burgonovo, 2012) allow forest management in the Atlantic forest under certain conditions, yet due to bureaucracy and lack of law enforcement, private landowners prefer to illegally exploit rather than use silvicultural prescriptions for Atlantic forest management. The most ecologically sound and widespread silvicultural prescription is liana cutting (Schnitzer and Bongers, 2002; Alvira et al., 2004; Pérez-Salicrup et al., 2004; Campanello et al., 2007). One half of flowering plant families contain lianas (Gentry, 1991), and their classification is typically based on morphology. Lianas may be divided into four groups, according to the mechanism type of host association (Hegarty, 1991): Scramblers; Twiners; Tendril climbers; and Root climbers. Lianas represent a large amount of plant diversity and are an important structural component in natural forests (Putz, 1983; Schnitzer and Bongers, 2002; Gehring et al., 2004; Letcher and Chazdon, 2009). Lianas affect trees by causing damages to bole and crown (Kainer et al., 2006), and by competing for resources, thus reducing value and increment of forest wood (Clark and Clark, 1990; Grauel and Putz, 2004; Campanello et al., 2007; Ladwig and Meiners, 2009; Ingwell et al., 2010). There is still some debate on whether trees are more affected by lianas in below-ground competition for water and nutrients, or in the above-ground competition for

T. Schröder et al. / Forest Ecology and Management 307 (2013) 84–89

light (Schnitzer and Bongers, 2002; Schnitzer et al., 2005). Lianas often increase in abundance in response to forest perturbation (Laurance et al., 2001; Schwartz et al., 2013), therefore their relative structural importance should increase in disturbed ecosystems such as the fragmented Atlantic rainforest. Liberating individual trees from lianas and tree competition are promising silvicultural components for improving tree growth and harvestable volume sustainability (Grogan et al., 2005; OhlsonKiehn et al., 2006; Wadsworth and Zweede, 2006). In this sense there are two approaches (De Graaf et al., 2003): light silviculture, in which wood production is carried alongside biodiversity conservation in the same area; and heavy silviculture, in which some areas of natural forest are domesticated for high-volume wood production, leaving other areas to be kept for biodiversity protection. Generalized liana cutting is controversial, once cut lianas may rapidly produce many new stems generating forests with a higher ramet density than prior to cutting (Parren and Bongers, 2001). Due to the widespread use of liana cutting in reduced impact logging, the majority of research relating tree growth and lianas is carried out on a liana presence/absence basis (Pérez-Salicrup and Barker, 2000; Campanello et al., 2007). But there is a long gradient of liana infestation when lianas are present in tree trunk or crown. Thus, there is no information regarding to how much different liana infestation affects the potential growth rate of trees free of lianas. Liberation from tree competition is a natural and dynamic process developed in the social environment of tropical forests (Wiersum, 1997). However, reducing tree competition for target trees to very low levels may reduce the capacity of the forest to protect the soil and the hydrological cycles. Besides, there is a considerable reduction in forest diversity and the forest may look degraded (Dekker and De Graaf, 2003). But due to the high resilience of tropical forests, the forest structure may recover in the time within one cutting cycle (de Graaf et al., 1999). As pointed out by Vidal et al. (1997) single tree species (or groups of species) silvicultural prescriptions would be a great step moving from forest exploitation to natural forest management. Parapiptadenia rigida Bentham (Brenan) (Fabaceae) is a common species in southern Brazil with high density wood (0.75–1 g/cm3) (Carvalho, 2003) ideal for internal and external floors, being virtually immune to termites. It is an early successional species characterized by its aggressive regeneration and growth, capable of forming nearly pure stand patches in Atlantic rain forest. This tree species follows the Troll crown architectural model proposed by Hallé et al. (1978). In this model, height growth is achieved through superimposed plagiotropic trunk axis. This is the most plastic crown architecture model, allowing trees to develop wide crowns when free of competition, and develop narrow crowns when under high competition. This architectural model occurs in virtually every tree in the Fabaceae botanical family. The aims of this study were: (1) to describe richness and diversity of liana species related to edge effects and P. rigida presence; (2) to assess sprouting differences among liana major morphological groups; (3) to quantify the effects of above- and below-ground liana competition on P. rigida growth; and (4) to develop liana management prescriptions for the target tree species in southern Brazil.

2. Methods 2.1. Site description The study site is located in the Central Depression of Rio Grande do Sul, Brazil. The site is occupied by is a 40–50-year-old forest that

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developed in an abandoned agricultural field (29°4000 2300 S 53°3700 5600 W); the largest trees already reached 100 cm dbh. The sloping terrain mainly has a northwestern aspect. The mean annual temperature is 25 °C with average temperature at 18 °C, with a maximum of over 30 °C in February. Mean annual rainfall is 180 cm, with no dry season, although water deficits are common during summer. The vegetation is classified as Subtropical Deciduous forest, with history of second-growth on abandoned agricultural fields in almost all fragments except for very steep areas. The fragment under study is dominated by P. rigida. 2.2. Field studies Field procedures took place in July 2011 (end of growing season). Liana sampling was carried out in one hundred subsample plots of 100 m2 (10  10 m) in a 5 ha fragment and followed the proposed standard protocol for liana censuses (Gerwing et al., 2006; Schnitzer et al., 2008). The centers of the plots were located from 5 to 60 m away from forest edge. Lianas larger than 2.2 cm were enumerated and measured, and all ramets belonging to the same individual were counted. The liana species were classified into four morphological groups proposed by (Hegarty, 1991), and divided into morpho-species. Voucher specimens were collected and subsequently identified through the collection of reproductive material made during field sampling and frequent checking of individuals during the following year. We selected 50 individuals of P. rigida inside the fragment, their diameters ranging from 10 to 50 cm. Two increment cores transversal to each other were extracted from each P. rigida tree, which is a suitable species for dendrochronological studies (Boninsegna et al., 1989). We measured diameter at breast height, the commercial height, total height and four crown radius for each individual. Tree competition was evaluated through the angle summation method (Spurr, 1962), which is a point basal area distance dependent estimate, ideal for natural forest spatial heterogeneity. As a measure of above-ground competition, liana crown cover was estimated using a five-point scale (van der Heijden et al., 2010), denominated Crown Occupancy Index (COI). As a measure of below-ground competition, all liana stems in a four meter radius circular plot (fifty plots equals 0.25 ha of total area) around P. rigida individuals were measured and identified. This radius was selected because it corresponded to the median of observed crown radius of P. rigida trees. 2.3. Data analysis Liana non-parametric species richness was estimated using Jackknife procedures (Burnham and Overton, 1978; Smith and van Belle, 1984), and diversity and evenness were calculated through Shannon and Pielou Index. The mean number of ramets per individual was compared among liana species using Tukey’s test, after natural logarithmic transformation (Loge) for homoscedasticity. Liana stems were divided into 10 diameter classes (Sturges, 1926), diametric distribution of different types of climbing mechanisms was compared in covariance analysis using exponential function for species with more than 15 individuals. Pearson’s correlation coefficient was calculated for liana density/liana basal area and edge distance. Liana basal area in the contiguous and circular plots was standardized to a hectare basis. The mean values for each species of liana community in the square and circular plots were compared with F test. Bartlett test was used to access homoscedasticity for each comparison and Loge transformation applied when needed. For competition description, liana basal area around P. rigida trees was discretized in basal area of scramblers (SBA) and basal area of lianas with special morphological adaptations to climbing

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(CBA). Correlation analysis was carried out among different liana competition indices, tree diameter and commercial height. A simple sigmoidal model was adjusted to the height:diameter ratio, Spurr basal area (SpBA) was included in the model, and then liana competition indices, number of liana stems (Nl), SBA, CBA and COI, were selected by stepwise regression. Increment cores of P. rigida were analyzed using the LINTAB– TSAP measuring system (RinnTech, Germany) with a precision of 1/100 mm. We used the last four growing years from each increment core. The previous tree diameter (winter of 2007) was obtained by subtracting the median of the two increment cores from measured diameter. The basal area increment (Vanclay, 1994; Peng, 2000) in the 4-year span was regressed against the 2007 tree diameter and SpBA, once again liana competition indices being selected by stepwise procedure. In any of the regression procedures, when COI was selected by stepwise procedure as the best competition measure, covariance analysis was used for model construction. Since tree diameter and growth increment did not contain zero or negative values, they were Loge transformed; Spurr point basal area and liana basal area were square root transformed since they may only assume non-negative values (Gelman and Hill, 2006). These transformations also guarantee model homoscedasticity (Monserud and Sterba, 1996). Data analysis was conducted using SAS software (SAS 9.2; SAS Institute Inc., Cary, NC); results were considered significant at p < 0.05. 3. Results Within the one hundred contiguous plots we found 1006 ± 782.4 liana stems (mean ± standard deviation) larger than 2.2 cm, corresponding to a basal area of 1.26 + 0.83 m2/hectare. The variation in number of stems (0.379, p < 0.01) and liana basal area (0.288, p < 0.01) were negatively correlated with distance from the edge, showing that liana abundance reduces with distance from forest edge. Tendril climbers represented 40.9% of lianas species, scramblers were 27.3%, twiners 22.7% and 9.1% of the total number of species were root climbers. Scramblers and tendril climbers had more ramets than other climbing mechanisms (Table 1). Liana diameter distribution varied among climbing mechanisms (Fig. 1). We found 23 liana species (Jackknife 1–2 = 25.9–27.9) in the contiguous plots (Shannon = 2.31; Evenness = 0.83) and 19 species (Jackknife 1–2 = 20.9–21.9) in the circular plots (Shannon = 2.01; Evenness = 0.75). More than half of liana species belonged to Bignoniaceae (7 species), Sapindaceae (3) and Fabaceae (2). The liana community was dominated by Senegalia tucumanensis (Fabaceae), which represented half of the total liana basal area. Liana stem number (F = 3.52, p < 0.06) and basal area (F = 6.91, p < 0.01) were larger in circular plots around P. rigida, but only two single liana species had differences in basal area: S. tucumanensis (Fabaceae) (F = 15.16, p < 0.01) with a larger basal area and Dasyphyllum

180

Number of lianas/ha

86

160

Scramblers

140

Tendrils

120

Root climbers

100

Twiners

80 60 40 20 0 2.5

4.5

6.5

8.5

10.5

12.5

14.5

16.5

Stem diameter (cm) Fig. 1. Results of covariance analysis examining effects of liana climbing mechanism on diameter distribution.

spinescens (Asteraceae) (F = 4.48, p < 0.04) with a smaller basal area in circular plots. Individual trees of P. rigida had 6.3 ± 3.4 lianas in a 4 m radius, corresponding to 2.11 ± 1.69 m2/ha of lianas. Mean crown occupancy was 28.8 ± 25.3%, with 18% of trees having no lianas on the crown. There was no correlation between diameter or commercial height and any liana competition index. Above-ground liana competition (measured by COI) was not correlated with below-ground competition (measured by liana basal area). The height:diameter ratio model explained most of height variation (F = 13.14; p < 0.01; R2 = 0.647), although tree point basal area was not significant (p < 0.15) it was kept in the model. COI (p < 0.01) was the best liana competition index explaining almost 6% of total height variation. Liana competition measured by COI affects tree diameter:height ratio (Fig. 2). Mean P. rigida annual diameter growth was 0.98 ± 0.38 cm with a maximum of 2.31 cm/year. The P. rigida basal area increment model explained most of the variation (F = 28.8; p < 0.01; R2 = 0.653). Once again tree point basal area (p < 0.19) was not significant but kept in the model. In this model, the best liana competition index (p < 0.02) was basal area of lianas with special morphological adaptations to climbing (CBA), explaining 5.35% of tree basal area increment. Liana and tree competition had large effects on individual tree growth of P. rigida trees (Fig. 3).

4. Discussion The higher number of tendril climber species showed a moderate successional status of the forest (Dewalt et al., 2000), although there is a great natural restoration of forest towards biomass, tree

3.2 3

Tukey grouping

B B B B B

A A A A A

C C C C C C C C

Mean number of ramets/individual

Species

Climbing mechanism

2.0 1.7 1.6 1.4 1.4 1.3 1.2 1.1 1.1 1.1

Celtis iguanaea Dasyphyllum spinescens Serjania laruotteana Tanaecium selloi Senegalia tucumanensis Serjania meridionalis Aristolochia triangularis Forsteronia glabrescens Anchietea pyrifolia Dolichandra unguis-cati

Scrambler Scrambler Tendrils Tendrils Scrambler Tendrils Twiner Twiner Twiner Root climber

2.8

Loge height

Table 1 Tukey’s test grouping for number of ramets per individual for liana species with more than 15 individuals.

2.6 2.4

4

3 2

2.2

1

5

2 1.8 0

0.02

0.04

0.06

0.08

0.1

0.12

1/Tree stem diameter Fig. 2. Results of covariance analysis for effects of crown occupancy index on height:diameter relationship.

Mean annual increment (cm)

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2.50 2.00 1.50 1.00 0.50 0.00

5

10

15

20

25

30

35

40

45

Diameter (cm) Fig. 3. Estimated mean annual diameter increment for Parapiptadenia rigida under mean and extreme values of tree and liana competition. Lower line represents diameter growth of trees under extremely high tree and liana competition (60 m2/ ha, 2.5 m2/ha) (point tree basal area, liana basal area, respectively). Mean competition is represented by the middle line (30 m2/ha, 0.5 m2/ha), and trees subject to extremely low competition (10 m2/ha, 0 m2/ha) had the highest predicted mean annual diameter increment.

and liana species composition remain at initial successional status (Tabarelli et al., 2010). Only 3.4% of the individuals remained without a conclusive botanical identification. The small number of liana species found on survey, when compared to other studies, shows the latitudinal gradient of shrinking plant diversity at higher latitudes (Clinebell et al., 1995; Ibarra-Manríquez and Martínez-Ramos, 2002; DeWalt et al., 2010) The high density of P. rigida in the study area is another relevant factor for small liana diversity. Even though the surveyed area in circular plots is smaller than the total area, the non-parametric richness estimators should overcome this difference. It is not clear through which mechanism the presence of P. rigida makes liana diversity lower, it could be explained by the larger dominance of S. tucumanensis in those sites, which increases competition for the same habitat with other lianas. Even though many studies have considered positive interactions among plants (Callaway, 1995; Brooker and Callaghan, 1998; Simberloff and Von Holle, 1999; Callaway et al., 2002), the explanation for most of these interactions remain unclear. Values here reported for liana density and basal area are close to those predicted by large geographical scale studies (Schnitzer, 2005; DeWalt et al., 2010). However, the values found around P. rigida are close to the maximums found in these studies and show the high spatial correlation between liana abundance and availability of suitable support (Schnitzer and Bongers, 2002; Malizia and Grau, 2006). Liana diameter distribution is influenced by the type of climbing mechanism, as root climbers are very distinct from other groups. While other groups follow the common inverse ‘‘J’’ shape distribution, this group, composed by two species of Dolichandra, presents individuals almost equally distributed in size classes, a behavior typical of light demanding plants (Kammesheidt, 2000). In fact, the yellow flowers of D. unguis-cati are a conspicuous spring feature in isolated trees alongside roads in southern Brazil, but this species is rarely found away from forest edges. D. uncata is a species that profusely regenerates in the understory, but is gapdependent. The vegetative capacity of liana species, measured by the number of ramets per individual, presented a pattern indicating greater resilience to liana cutting by scramblers and tendril climbers. The higher number of ramets in scramblers is explained by the lack of special climbing mechanisms, thus a higher number of ramets increases the chances to find suitable supports. On the other hand, once attached to a host tree and with light availability, extremely

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specialized root climbers show a lower chance of mortality, being attached to the remaining life span of its host tree. Species with high vegetative reproduction should be submitted to more aggressive liana control methods, such as the two-point cutting (PerezSalicrup et al., 2001), in which lianas stems are cut at ground level and shoulder level, avoiding their old stem, a readily available support for lianas. This reduces fast reoccupation of the habitat by liana sprouts and waste of financial resources. A common feature of forest fragments and edges is the increased liana abundance (Laurance et al., 2001) and it has been proposed as one cause of greater tree mortality in these ecosystems (Laurance et al., 2000). Our data support the pattern for larger liana basal area and number of liana stems in such forest typologies. If the high liana abundance on forest edges reduces tree growth, on the other hand liana stems and leaves create a barrier that reduces the entrance of light and wind in the forest interior, increasing environmental stability inside the fragment (Engel et al., 1998). Thus, liana presence along edges improves habitat suitability for late successional species regeneration. Therefore, decision regarding liana cutting in forest edges habitats should rely on ecological information about regeneration of commercial species of the area under management. If the highest income from forest management comes from light demanding species, lianas should be heavily controlled in fragment edges. We found no correlation between tree commercial height or diameter and liana competition. It was suggested that liana infestation is correlated to tree diameter (Clark and Clark, 1990; Campanello et al., 2007), since larger diameters indicated longer exposure to liana community and crown/trunk occupation. Another relationship proposed is that lower tree commercial heights generate more readily available supports to liana development (Campanello et al., 2007). Our study did confirm these relationships because P. rigida trees are distributed in a liana abundance gradient controlled by edge distance, thus liana infestation is controlled by tree position within the fragment (liana abundance) rather than tree dimension (Malizia and Grau, 2006). The lack of correlation between belowand above-ground liana competition indices (Van Der Heijden and Phillips, 2009) (but see (Clark and Clark, 1990; Kainer et al., 2006)) demonstrates the capacity of lianas to move laterally in forest canopy, making it irrelevant whether lianas are rooted in the plot or not (Schnitzer and Bongers, 2002; Gerwing et al., 2006). The height:diameter model showed a clear tendency of trees growing with liana COI over 50% having a lower height:diameter ratio. This is due to the plastic crown architecture of P. rigida (Hallé et al., 1978). When lianas overtop the highest leaves of this species, reducing light availability, P. rigida tree crowns starts to develop laterally. Once about 80–95% of the area of a natural forest is occupied by tree crowns (Assmann, 1970), when the tree finds these canopy blank spots, it is able to maintain diameter growth and increasing survival rate under high liana competition in comparison to other crown architecture schemes. Below a COI of 50% the height:diameter ratio increases compared to liana free trees. It is known that competition increases the height:diameter ratio in pure even aged forests (Assmann, 1970), but this trend is harder to find in natural forests due to botanical and spatial heterogeneity. For trees with less than half of the crown occupied, liana competition has the same effects as tree competition, increasing height:diameter ratio up to a maximum around 25% of COI. This showed that tree and above-ground liana competition are not different for the subject species, because they are just woody plants competing for light. Individual tree basal area growth was mainly explained by its own dimension, and less by competition, and the same trend was found by Monserud and Sterba (1996). Liana basal area is a good auxiliary variable to explain tree growth variation (Clark and Clark, 1990; Ladwig and Meiners, 2009; Van Der Heijden

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and Phillips, 2009). Overall the variation explained by liana below-ground (measured by liana basal area) competition in this study was higher than normally reported (Ladwig and Meiners, 2009; Van Der Heijden and Phillips, 2009). This distinction is due to the methodological approach; these studies used a onemeter radius plot around individual trees as an estimation of liana below-ground competition, which is highly unlikely to represent tree root development for trees much larger than 10 cm of diameter. The 4 m radius used is similar to the area of the plot applied in previous studies to quantify above-ground liana competition, defined by lianas clearly climbing to tree crown. However, this implies a high correlation between ground level liana basal area and liana leaf mass on the tree crown, and that is a weak relationship due to liana lateral growth in forest canopy.

5. Conclusions and recommendations Lianas high abundance in the fragment under study showed the relation between this group of plants and human disturbance in the Atlantic rainforest. In a rough comparison to a canopy tree survey in a nearby forest area (Budke et al., 2004), lianas are responsible for 30% of the forest canopy species richness. Thus, its control as a silvicultural treatment for forest management should be carefully planned in order to maintain the overall forest diversity. Areas near forest edges are especially problematic in the decision-making about liana cutting; these patches should be managed in order to increase forest value in a long-term goal. Natural forest management is a low-profit activity in Brazil (Boltz et al., 2001; De Graaf et al., 2003), thus there should be careful planning of silvicultural treatments in order to avoid waste of time and resources. Liana cutting should be applied on a tree by tree basis (Schnitzer and Bongers, 2002), liberating only commercially valued species. Our results showed that below-ground liana competition decreases tree growth continually, but this is a nonoperational variable for field decisions about liana cutting. Considering an interval of 5–10 years between silvicultural treatments (De Graaf et al., 2003), the results found in the height:diameter ratio, and liana crown occupation capacity (van der Heijden et al., 2010), even in heavy silviculture management programs, were that lianas should be cut in all P. rigida trees with diameter smaller than 20 cm. For larger trees, lianas should only be cut when more than 25% of tree crowns were occupied by them. Cutting all lianas in the forest is not recommended because it selects towards more aggressive genotypes (Engel et al., 1998). The model developed for tree diameter growth showed a good capacity to explain basal area increment variation. The use of this model to predict diameter increment in P. rigida trees subject to different levels of tree and liana competition shows that the use of silvicultural treatments could increase mean annual diameter increment to about 1.5 cm/year. The tree species under study, P. rigida, presents features that are rarely found in the same species, which are the fast growth and high-density wood. For this reason, this species becomes ideal for forest restoration and carbon sequestration.

Acknowledgments We would like to thank CAPES – Coordination for the Improvement of Higher Education Personnel, which supported this study. Suzane Saldanha and Noé dos Santos Hofiço were of great help with the English writing. A special thanks to the anonymous reviewers who provided very thoughtful comments for the development of this manuscript.

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