CARBON STOCK GROWTH IN A SECONDARY ATLANTIC FOREST

– The secondary Atlantic forests play an important role in the context of climate change, acting as a carbon sink for the atmosphere. However, these forests can become a carbon source in case of increased tree mortality. Knowing this change is possible through continuous forest inventories that provide information on the dynamics of tree growth. Thus, the objective of this study was to evaluate the carbon growth dynamics of a Seasonal Semideciduous Forest fragment, with 44.11 ha, located in the Parque Tecnológico de Viçosa – MG. The forest inventories were carried out in twenty plots of 10 m x 50 m, in the years of 2010 and 2015, where all stems with dbh ≥ 5 cm were measured, botanically identiﬁ ed and classiﬁ ed in ecological groups. The stem volume was obtained through volumetric equation. Biomass and carbon stock were quantiﬁ ed for compartments located above the ground (stem, branches and leaves) and below ground (roots). The dynamics of carbon growth were evaluated by Gross Increment (GI) and Periodic Annual Increment in carbon of the species (PAI). The GI was 12.72 MgC ha -1 , including the carbon from the stems that were recruited and died during the monitoring period. The carbon stock increased 10.01 MgC ha -1 , resulting in an PAI of 2.00 MgC ha -1 year -1 . Thus, it is concluded that the forest fragment present positive carbon stock growth due to successional progression, ratifying the importance of secondary forest of the Atlantic forest in the mitigation of greenhouse gases in the atmosphere.


INTRODUCTION
The Atlantic Forest has one of the richest biodiversities in the world, hosting a range of animal and plant species (Joly et al., 2014;Fundação SOS Mata Atlântica and INPE, 2018). This biome also provides a wide range of ecosystem services (Bullock et al., 2011;Ruggiero et al., 2019), such as carbon storage in the multiple compartments of trees and soil (Pan et al., 2011;Delgado et al., 2018).
The Atlantic Forest is able to stock approximately 94.70 MgC ha -1 in the arboreal individuals, leaving behind only the forests of the Amazonian biome in Brazil (FAO, 2014). In the specifi c case of seasonal semideciduous forests, recent studies have estimated that carbon stocks in trees can range from 30.99 MgC ha -1 (Torres et al., 2017) to 55.91 MgC ha -1 (Silva et al. 2018).
However, the increase of natural disturbance intensity and frequency caused by climate change, such as storms and droughts (Malhi et al., 2008;IPCC, 2014;McDowell et al., 2018) can transform these forests from sink to carbon source for the atmosphere (Malhi et al., 2014;Teixeira et al., 2015;Lu et al., 2019). In this scenario, the tree mortality increase in the leads to a higher carbon loss, surpassing the stock in new individuals and also the growth of remaining trees in a specifi c period of time (Phillips et al., 2009;Aleixo et al., 2019).
Knowing this change is possible through continuous forest inventories that provide information on the dynamics of forest growth Teixeira et al., 2016). Besides, the study of the growth dynamics also allows inferring about the transformations occurred in the structures and the fl oristic composition of the forest (Figueiredo et al., 2013;Meyer et al., 2015) as well as assessing health and the probable impacts from the climate change (Brodie et al., 2012).
In the Atlantic Forest, few studies have attempted to indicate if the forest is acting as a sink or source of carbon for the atmosphere through the growth dynamics (Figueiredo et al., 2015), being the most part restricted in simply estimating the carbon stock (Torres et al., 2013;Carvalho et al., 2015;Diniz et al., 2015). Given this scientifi c gap, this study aimed to evaluate the dynamics of carbon growth of a secondary forest fragment of the Atlantic Forest.

Description of the Study area
The forest fragment size is 44.11 ha and it is located in the Parque Tecnológico de Viçosa -MG, whose geographical coordinates are 42° 51' W and 20° 42' S (Torres et al., 2013) in an average altitude of 721 m (Souza et al., 2014). Its vegetation can be classifi ed as Montana Semideciduous Seasonal Forest (IBGE, 2012). According to the CONAMA resolution 392, the fragment is in the middle stage of regeneration, displaying woody species with an average dbh between 10 and 20 cm, and height between 5 and 12 m (Brazil, 2007).
The local climate is the Cwa type, in the Köppen classifi cation. The average temperature, humidity, and annual rainfall from 1968 to 2015 is 21.9 °C, 79% and 1,274 mm, respectively (UFV, 2016). The region of Viçosa has pedogeomorphologic gradients with aluminum-rich dystrophic latosols at the tops of hills, colluvial ramps with shallow latosols and cambic horizon, while the bottoms of the groves present a predominance of epieutrophic cambisols rich in nutrients (Ferreira Júnior et al., 2012). Several disturbances have occurred over the years in this forest fragment, such as removal of wood and insertion of agricultural crops and eucalyptus. However, about 25 years ago, it has been occurring the regeneration of its native vegetation (Torres et al., 2013).

Data collection and Analysis
Twenty plots (10 m x 50 m) were inventoried, in 2010 and 2015, in which all individuals that showed dbh ≥ 5 cm were measured and botanically identifi ed. When necessary, the Missouri Botanical Garden (2016) was checked to confi rm the scientifi c names of these species.
The species were classifi ed into ecological groups according to the division proposed by Gandolfi et al. (1995) and used in other studies such as Callegaro et al. (2015), Figueiredo et al. (2013) and Figueiredo et al. (2015), in which they were presented as Pioneer (P), Early Secondary (ES), Late Secondary (LS) and species without classifi cation (SC).
Mortality was recorded in 2015, which corresponds to the individuals that are alive in a specifi c moment, but are found dead on a second one; and recruitment, which are individuals who reach a minimum inclusion diameter (dbh ≥ 5cm) in the last measurement. The recruitment and mortality rates were calculated by the methodology proposed by Ferreira et al. (1998).
The tree component volume was predicted using the equation VF cc =0.000070*DBH 2.204301 * H t 0.563181 (R 2 = 97.04% and S yx =17.4%), in which: VF cc = stem volume inside bark (m 3 ), DBH = diameter at breast height (cm) and H t = total height (m), adjusted to trees in a Montana Semideciduous Seasonal Forest, located in Viçosa -MG (Amaro, 2010).
For the stem biomass and carbon stock quantifi cation, three trees per specie and diameter class size were selected. Wood samples were removed at 1.30 m using increment borers. Afterwards, some of the materials were taken to the laboratory to have their wood basic density determined, according to the methodology described by Vital (1984) and NBR 11941 (2003), and the other part was subjected to complete calcination in an muffl e furnace to determine the carbon content, according to the methodology described by Torres et al. (2013).
For the branch biomass quantifi cation, a conversion factor = 0.2596 to convert stem biomass inside bark to branch biomass was used (Amaro, 2010;Amaro et al., 2013;Torres et al., 2013). Conversion factor equal to 0.0445 was used for the foliage component (Drumond, 1997;Amaro et al., 2013;Torres et al., 2013). In both cases, the carbon stock was obtained by multiplying the biomass by 48.54%, which corresponds to the average carbon content found by Amaro (2010) for the same forest typology.
For the roots, it was considered that this component corresponds to 24% of the stem biomass (Amaro et al., 2013;Torres et al., 2013). The carbon stock was quantifi ed considering the same content used for the branches and leaves. This way, the total carbon stock of the fragment for 2010 and 2015 was obtained by the sum of the carbon stock above the ground (stem, branches, leaves) plus the carbon stock below the ground (roots).
The Gross Increment (GI) in carbon of the forest fragment (growth) was obtained through the equation: GI = (C f -R) -(C i -M), in which: GI = gross increment, excluding the recruitment, in MgC ha -1 ; C f = carbon stock at the end of the period, in MgC ha -1 ; C i = carbon stock at the beginning of the period, in MgC ha -1 ; R = recruitment of stems, resulting in the growth of stored carbon, in MgC ha -1 ; M = mortality of stems, resulting in loss of stored carbon, in MgC ha -1 (Davis;Johnson, 1987;Figueiredo et al., 2015).
The Periodic Annual Increment in carbon (PAI), by species, was calculated by the following equation: PAI = (C f -C i ) / t, in which: PAI = periodic annual increment per species, in MgC ha -1 ano -1 ; C f = carbon stock at the end of the period, in MgC ha -1 ; C i = carbon stock at the beginning of the period, in MgC ha -1 ; t = time gap, in years. The Periodic Annual Increment in carbon per stem was calculated through the following equation: PAI stem = PAI / SD i , in which: PAI stem = periodic annual increment per stem, in MgC stem -1 year -1 ; SD i = stems density of each species, in stems ha -1 (Figueiredo et al., 2015).

RESULTS
During the monitoring period (2010)(2011)(2012)(2013)(2014)(2015), the total number of stems ha -1 increased from 1526 to 1692 (Figure 1), including the mortality of 169 stems ha -1 and the recruitment of 335 stems ha -1 . This way, the mortality rate of the studied species was 2.00% each year, while the recruitment rate was 3.96% each year.
The biomass and the carbon stock had an increase of 19.51 Mg ha -1 and 10.01 MgC ha -1 , respectively, during the assessed monitored period (Table 1).
The carbon accumulation was higher in the early secondary species and in the fi rst diameter classes. In this ecological group, the carbon accumulation was 5.77 MgC ha -1 , while for the pioneer, unclassifi ed, and late secondary species, it was 2.86 MgC ha -1 , 0.53 MgC ha -1 and 0.85 MgC ha -1 , respectively ( Table 2).
The Gross Increment (GI) in carbon of the forest fragment (growth) was 12.72 MgC ha -1 , considering carbon lost by mortality and carbon stocked by recruitment ( Figure 2).

DISCUSSION
In the observed period (2010)(2011)(2012)(2013)(2014)(2015), the number of individuals recruited (335 stems ha -1 ) was higher than mortality (169 stems ha -1 ), corresponding to a rate of 3.96% and 2.00% per year, respectively. When we analyze the Figure 1, the stems mortality was observed in the last diameter classes, while the recruitment occurred mainly in the fi rst classes. Moreover, there was an increase in the number of stems ha -1 in this period, from 1526, in 2010, to 1692, in 2015. This growth dynamic of the forest fragment was driven mainly by intrinsic factors to the community, such as topography and geology of the place, the species characteristics and the forest successional stage (Xu et al., 2016;Ma et al., 2016). Due to the short monitoring time, it was not possible to notice the contribution of the climatic factors, despite being present in this process (Kardol et al., 2010;Zhang et al., 2015).
In terms of biomass and carbon, an increase of 19.51 Mg ha -1 and 10.01 MgC ha -1 , respectively, was observed in the monitoring period. This increase in the accumulation of biomass and in the carbon stock is justifi ed by the forest successional (Souza et al., 2012), leading to a greater richness of non-pioneer species with higher wood density (Fonseca et al., 2011;Shimamoto et al., 2014). This is corroborated by Diniz et al. (2015) who, when studying two fragments of Submontana Semideciduous Seasonal Forest, obtained a carbon stock of 20.9 MgC ha -1 for the forest during middle succession stage and 70.6 MgC ha -1 for the forest during advanced succession stage. In case of Souza et al. (2012), they found a carbon stock of 36.54 MgC ha -1 and 75.25 MgC ha -1 for fragments of Submontana Semideciduous Seasonal Forest during middle and medium/advanced stages, respectively. Thus, it is expected that, over the years, the fragment may increase its capacity to store carbon until the forest ecosystem enters a dynamic balance (Oliveira et al., 2014).

Species
This upward stock contributed to carbon growth of the fragment, that was 12.72 MgC ha -1 . Of this total, about 60% was due to the growth of the early secondary species (Figure 2). This ecological dominance of early secondary species on carbon growth was also a refl ection of the successional progression of the forest fragment.
Considering the period evaluated (2010 to 2015), it was found a periodic annual increment in carbon (PAI) of 2.00 MgC ha -1 year -1 . In a study by Figueiredo et al. (2015), in a semideciduous seasonal forest, in the middle stage of regeneration, it was found an estimate of PAI in carbon of 0.994 MgC ha -1 year -1 , from 1994 to 2008, considering only the stem. Souza et al. (2011) found an PAI in carbon of 0.14 MgC ha -1 year -1 for a semideciduous seasonal forest, also in the middle stage of regeneration, from 2002 to 2007, considering stems and branches. The PAI estimates found by these authors were much lower than those found in this study. One of the causes that may have infl uenced this low PAI is the non-quantifi cation of components, such as leaves and roots, to which they are relevant in the carbon stock of tropical forests (Watzlawick et al., 2012;Torres et al., 2013).
The PAI in carbon by species indicated that Piptadenia gonoacantha (P), Anadenanthera peregrina (ES), Myrcia fallax (ES), Matayba elaeagnoides (ES) and Sparattosperma leucanthum (ES) distinguished themselves in relation to other species. Together, these fi ve species accounts for 33% of the fragment's PAI. The knowledge over the species that have the greatest potential in storing carbon allows to guide forestry managers on fl oristic composition, in forest restoration projects or in carbon neutralization plantations in regions whose soil and climatic conditions are similar to that of the studied fragment. This way, the mitigation capacity of these areas can be intensifi ed, making them large atmosphere carbon sinks.

CONCLUSIONS
The trees of the forest fragment had carbon stock growth (2.00 MgC ha -1 year -1 ) due to successional progression. The species that most contribute to the removal of carbon are Piptadenia gonoacantha, Anadenanthera peregrina, Myrcia fallax, Matayba elaeagnoides and Sparattosperma leucanthum. This fact corroborates that, even in the face of climate change, the secondary Atlantic Forests play an important role as a carbon sink and, consequently, in the reduction of the greenhouse gas concentration in the atmosphere.

ACKNOWLEDGEMENT
We would like to thank the Conselho Nacional de Desenvolvimento Científi co e Tecnológico (CNPq), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the research funding. We would also like to thank the study group in economy and forest management (GEEA) for their assistance with data collection. To the Parque Tecnológico de Viçosa and CENTEV for the concession of the study area.