MYRACRODRUON URUNDEUVA FR ALL. (AROEIRA TREE) POPULATION DYNAMICS, DIAMETER GROWTH RATE AND ITS POTENTIAL FOR SUSTAINABLE MANAGEMENT IN SUCCESSIONAL TROPICAL DRY FORESTS OF BRAZIL

Sofia Calvo Rodriguez, Julio Calvo Alvarado, Mario Marcos do Espírito-Santo, Yule Roberta Ferreira Nunes 1 Received on 14.06.2016 accepted for publication on 24.05.2017. 2 Earth and Atmospheric Sciences Department, University of Alberta, Edmonton, Alberta, Canada. E-mail: <calvorod@ualberta.ca>. 3 School of Forestry, Costa Rican Institute Of Technology,Cartago, Costa Rica. E-mail: <jucalvo@itcr.ac.cr>. 4 Universidade Estadual de Montes Claros, Doutorado em Ecologia, Montes Claros, Minas Gerais, Brasil. E-mail: <marioesanto@gmail.com> and <yule.rfnunes@gmail.com>. *Corresponding author.


1.INTRODUCTION
Myracrodruon urundeuva Allemão (Anarcadiaceae), which is better known in Brazil as the "Aroeira tree", is a xerophytic deciduous tree species (Lorenzi, 1992;Nunes et al., 2008).The "Aroeira tree" is a secondary, pioneer species, which is usually rare in primary forests, but common in disturbed areas (Ferretti et al., 1995).The species has been classified by Linares-Palomino et al., (2011) as a specialist of the tropical dry forests.
M. urundeuva is a sizeable tree with heights between 20 and 30 meters (Oliveira-Filho et al., 1998).The wood of this species is reddish-brown with a density of 1.00 to 1.21 g/cm³ (Bertoni and Dickfeldt, 2007).The hardness of the wood makes it economically valuable, and it is widely used in rural areas for construction that requires external resistance and durability, such as sheds, fences, poles, and sleepers (Medina, 1966;Rizzini, 1971Rizzini, , 1995;;Nogueira, 1977;Carvalho, 1994;Bertoni and Dickfeldt, 2007).This tree also has pharmacological uses.Its bark has anti-inflammatory, astringent, anti-allergic, and healing properties (Viana et al., 1995;Nunes et al., 2008).The roots are used for treating rheumatism, and the leaves are used to treat ulcers (Almeida et al., 1998;Nunes et al., 2008).Extracts of leaves exhibit strong antioxidant activity and moderated antimicrobial activity (Mota et al., 2015).M. urundeuva wood has also proved to be resistant to microorganisms given the fungicidal and antibacterial properties found in its heartwood (Sá et al., 2009).
Like other species with valuable characteristics and high economic value, M. urundeuva has suffered from indiscriminate logging in Brazil, which has compromised their natural populations in some locations to the point where the species has been reported in the past as endangered (Bertoni and Dickfeldt, 2007;Brasil, 2008).The species was considered in the "Brazilian Report on Forest Genetic Resources" in 2012 (FAO, 2012) as a prioritized tree species for genetic conservation and research initiatives in Brazil given its economic value.
In spite of the high commercial value of this species, due to the excellent wood properties and its potential pharmacological use, at present there are no studies analyzing the recovery time and growth of this species in different stages of forest succession in the Brazilian tropical dry forest.This type of analyses can help us understand the value of these forests, improve forest management practices and develop growth models that could help to assess its performance and adaptability for silvicultural management under different environmental conditions.
Previous studies conducted by our research network (TROPI-DRY, Sánchez-Azofeifa et al., 2005a,b;2013), revealed that the species M. urundeuva has a high density of stems and a high rate of diameter growth in the early successional stage (Calvo-Rodriguez et al., 2017a).However, researchers in Brazil, urge more investigations on the dynamics of M. urundeuva populations to make inferences about harvest sustainability more accurately (Barros et al., 2016).For this reason, we would like to contribute to the preservation of this species and the tropical dry forest of Brazil, by attempting to demonstrate that this species is a fast-growing valuable tree that has the potential to be harvested in sustainable silvicultural treatments.Consequently, the pressure suffered by the demand on this species could be lessened by obtaining timber and pharmacological products from tree plantations, agroforestry systems or sustainable natural forest management.In the same manner, silvicultural management of this species can enhance the restoration and conservation of tropical dry forest in Brazil.Therefore, Myracrodruon urundeuva fr all... the main objectives of this study were to determine and compare the mortality, recruitment and growth rates in diameter of this species in three successional stages of a tropical dry forest.

Study site
The study was conducted in Mata Seca State Park (MSSP), currently managed by the Forestry State Institute (IEF-Instituto Estadual de Florestas).MSSP has an area of 15,466 hectares at an elevation of 452 m.a.s.l and is situated in the São Francisco river valley, in Minas Gerais state in Brazil.The exact location is between coordinates 14°48'36" -14°56'59" S and 043°55'12" -044°04'12" W (Calvo-Rodríguez, 2017a; Silva et al., 2015).The local climate is considered tropical semiarid (Köppen classification) or tropical dry forest (Holdridge classification).The forest is dominated by deciduous trees that lose almost 90-95% of their leaf area during the dry season that extends for six months between May and October (Madeira et al., 2009).The average temperature of the study area is 24.4°C with a maximum of 32°C and a mean annual precipitation of 871mm (300-1300mm range), with a rainy season from October to April (Calvo-Rodríguez, 2017b; Silva et al., 2015).

Experimental design
In MSSP, 18 permanent plots were established in the three successional stages of the forest: early, intermediate, and late (6 plots per stage).Each plot has an area of 1.000 m 2 (50x20m).In each plot, we measured annually the diameters of all individuals of all species with a diameter greater than 5 cm at breast height (1.3 m) including the species M. Previous studies (Calvo-Rodríguez et al., 2017b) for these plots showed that M.urundeuva (Anacardiaceae) had the greatest ecological weight, with an IVI of 99.06 (Importance Value Index, Curtis and McIntosh, 1951), in the early successional stages.This species had the second highest IVI in the late stage with 31.57and, although it was not among the most significant in the intermediate forest, it was also present in this stage.

Data analysis
With the data from each successional stage, we proceeded to calculate for each individual the diameter in millimeters and the basal area per hectare in square meters for 2006 and 2014.Then we calculated the mean annual increment in mm/year (MAI) for M.urundeuva only for those individuals that were present in the measurements between 2006 and 2014.To calculate the MAI for each tree, we divided by 8 (number of years from 2006 to 2014) the incremental difference of the diameters from 2006 to the year 2014.For the statistical comparison of MAI among successional stages, we used the median instead of the arithmetic average, because the data do not have a normal distribution, and the use of the median decreases the bias caused by extreme values (Ortiz and Carrera, 2002;Carvajal-Vanegas and Calvo-Alvarado, 2013a,b).Because of this non-normal distribution, we used the Kruskal-Wallis non-parametric statistical test (Kruskal and Wallis, 1952).
Tree mortality (m), recruitment (r), were calculated using a logarithmic model (Lieberman and Lieberman, 1987;Sheil et al., 1995;Condit et al., 1999;Carvajal-Vanegas and Calvo-Alvarado, 2013a,b).The mortality and the recruitment in each successional stage were calculated using the following formulas: where N 06 is the number of individuals present in 2006, N S is the number of individuals surviving in 2014, and for recruitment, N 14 is the number of individuals surviving in 2014 plus the number of individuals recruited during the time period T.

3.RESULTS
We tallied 108 individuals of this species within the 18 plots in 2006 and 271 individuals in 2014 (Table 1).Mortality rates were higher in the early and intermediate stage (7.4% and 8.2% respectively) and recruitment rates were higher in the early stage (22.9%).
In total, 97 trees were chosen within the 18 plots for the analysis of growth among the three successional stages.The largest MAI was in the early stage (10.53±3.77mm/year, n= 62), which was significantly different (p<0.05)EQ1.
This species attained a maximum increment of 17.91 mm/year in the early stage, while in the intermediate and late stages it only reached maximum increments of 4.38 mm/year and 9.30 mm/year, respectively.Most of our measurements of MAI were between 2-14 mm per year (Figure 1).The median of the total population was 8.15 mm/year for all forest successional stages.The species is found in all diameter classes from 5 cm-65 cm (Figure 2), but maximum increments were obtained in the diameter classes 5-15 cm and 15-25 cm in the early stage.For the intermediate stage, maximum increments were found in the 5-15 cm diameter class and, for the late stage, in the 35-45 cm class.

4.DISCUSSION
Recruitment and mortality rates were higher in the early and intermediate stages than in the late stage of succession.It is expected that at lower diameter classes, there is intense competition for space and resources, because of the wide variety of species and individuals that seek to establish themselves in this ecosystem (Monge et al., 2002).Also, the results strongly suggest that M. urundeuva has its most rapid diameter growth rate within the early successional stage.According to Vieira et al., (2007), this species grows more rapidly where there is more light exposure than it does in forests with less disturbance.
In the early successional stage, M. urundeuva has a rapid incremental growth in diameter (MAI=10.53mm/year), indicating that in this stage the species could reach diameters of 12-20 cm in 10-15 years.This diameter range is very acceptable for harvesting trees for rural use, for non-wood forest products and for the small diameter wood industry (Keegan et al., 2004;Bermúdez-Cruz et al., 2006).Our results are comparable with those obtained by Bertoni and Dickfeldt, (2007) in Brazil, who showed that this species was effective in restoring a disturbed area, by obtaining a diameter of 8.25 cm, a height of 7.20 m, and a survival rate of 90% over ten years.
In the intermediate and late successional stages, the MAIs are very slow, which is normal for a species with a high wood density, and hence it will take several years to reach larger diameters.Venturoli et al., (2015)   Myracrodruon urundeuva fr all... found annual increments of 1.4 to 3.3 (mm/year) for this species in a semideciduous secondary forest in Goiás, Brazil.In this study, they analyzed annual increments of species with the highest importance value index, under treatments such as removal of all woody individuals within a radius of one meter from the desirable trees, removal of all large lianas in the plot and, introduction of seedlings.Greatest increments of M. urundeuva were observed in the plots where the three treatments were applied (Venturoli et al., 2015), showing that this species responded positively to silvicultural interventions.
Although this species grows in secondary forests, its rate of growth is also comparable to commercial species established in plantations, where growth is optimized, and there is even a genetic selection.For example, our results compare very well with MAIs reported for Teak plantations at several sites across Central America.Specifically, for sites with the same climatic conditions (Tropical dry forest, Life Zone) as in our study where MAIs were reported, growth rates in three different teak plantations in Panama were 10 -15 mm/ year (Chaves and Fonseca, 1991).The MAIs of M. urundeuva in natural forest are even higher than the increments of other valuable tropical tree species for the dry forest, such as mahogany (Swietenia macrophylla King).Grogan, (2001) found in southern Pará (Brazil) MAIs between 4.9 mm/year and 7.9 mm/ year for mahogany trees with DBH greater than 10 cm.
While in Quintana Roo, Mexico, Negreros-Castillo and Mize (2014) found for mahogany trees with a DBH > 10.0 cm MAIs of 2.2 mm/yr on average and maximum MAIs of 19.7 mm/yr.

5.CONCLUSION
Results from this study support the conclusion that this tree is not only a pioneering species, but that it also tolerates the conditions of advanced successional stages.Highest diametric increments were observed in the early stage of succession and in the smaller diametric classes.Intermediate and late succession plots also had considerable diametric increments, however, these were significantly lower than the early stage.Because of its excellent wood properties, its pharmacological potential, the high tree density, and high diameter growth rates found in this study, especially in the early successional stage, we also conclude that the "Aroeira tree" should be studied to become a flag species for silvicultural management of the tropical dry forest of Brazil and to be a domesticated tree for agroforestry and forest plantations systems.

Figure 1 -
Figure 1 -Distribution of the mean diameter annual increments (MAI, as median in mm/year) and minimum and maximum values observed for Myracrodruon urundeuva in three successional stages in Mata Seca State Park, Minas Gerais Brazil.Figura 1 -Distribuição de média de incrementos anuais (MAI, como mediana em mm/ano) e valores mínimos e máximos observados para Myracrodruon urundeuva em três estádios sucessionais no Parque Estadual Mata Seca, Minas Gerais Brasil.
part of the Research Project: TROPI-DRY (Human, Ecological and Biophysical Dimension on Tropical Dry Forest) a collaborative research network funded by the Inter American Institute for Global Change Research (IAI) Collaborative Research Network Program (CRN2-021), supported by the U.S. National Science Foundation (Grant GEO 0452325).We also received support from the Costa Rican Institute of Technology (ITCR), University of Alberta, Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).7.REFERENCES Almeida SPD.Cerrado.Planaltina, DF: Empresa Brasileira de Pesquisa Agropecuaìria, Centro de Pesquisa Agropecuaìria dos Cerrados, Ministério da Agricultura e do Abastecimento; 1998.Alvarez M, Avila-Cabadilla LD, Berbara R, Calvo-Alvarado JC, Cuevas-Reyes P, Espírito-Santo MM et al.Ecology procedures.In: Nassar JM, Rodríguez JP, Sánchez-Azofeifa GA, Garvin T, Quesada M editores Manual of methods: human, ecological and biophysical dimensions of tropical