Geoderma Regional xxx (2019) e00218

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Carbon and nitrogen stock of Acrisols and Nitisols in South Bahia, Brazil

Camila V. Oliveira a, Laís C. Vicente b, Emanuela F. Gama-Rodrigues a,b,⁎, Antonio C. Gama-Rodrigues b,José R.B. Marques c, Patrícia A.B. Barreto-Garcia a

a Universidade Estadual do Sudoeste da Bahia/UESB, Vitória da Conquista, BA CEP 45083-900, Brazilb Universidade Estadual do Norte Fluminense Darcy Ribeiro – UENF, Campos dos Goytacazes, RJ CEP 28013-602, Brazilc Comissão Executiva do Plano da Lavoura Cacaueira – CEPLAC/Centro de Pesquisas do Cacau – CEPEC, Km 22, Rodovia Ilhéus, Itabuna, BA CEP 45700-000, Brazil

⁎ Corresponding author at: UENF/CCTA/Soil LaboratoCampos dos Goytacazes, RJ CEP. 28013-602, Brazil.

E-mail address: emanuela@uenf.br (E.F. Gama-Rodrigu

https://doi.org/10.1016/j.geodrs.2019.e002182352-0094/© 2019 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 7 August 2018Received in revised form 21 March 2019Accepted 26 March 2019Available online xxxx

This study evaluated if the effect of secondary forest (SF) conversion into pasture (PAS) or rubber tree plantation(RT) and cacao+erythrina AFS (C+E) conversion into cacao+ rubber tree AFS (C+RT) on the C andN storagein soils and aggregate-size fractions could be compensated by a high amount of organic residues deposited overthe years by rubber tree plantation and agroforestry systems (above and belowground) and a high amount ofbelowground residues deposited by pasture. Soil samples were collected from six layers (0–10, 10–20, 20–40,40–60, 60–80 and 80–100 cm) and separated by wet-sieving into three fraction-size classes (2000-250 μm;250-53 μm and b 53 μm) in soils under RT, PAS and SF sites (Argisols) and C + RT and C + E AFSs (Nitosols).The C and N were determined by dry combustion. The average soil organic carbon (SOC) stock in Acrisols was207 Mg ha−1 up to 100 cm depth, and 72 Mg ha−1 was stored at the first 30 cm depth; while the average SOCstock in Nitosols was 224 Mg ha−1 up to 100 cm, and 116 Mg ha−1 at 30 cm depth. As expected, C and N stockin soils and in the different soil aggregate-size fractions revealed that the dissimilarity between siteswas stronglyinfluenced by soil order. There was high dissimilarity between the sites in Nitosols and those in Yellow Argisols,and the dissimilarity between the land use systems only occurred in the Yellow Argisol. The conversion effect ofcacao+erythrina AFS into cacao+ rubber treeAFSwas restricted to the surface soil and did not promote dissim-ilarity among the AFSs regarding the C and N storage in the whole soil and aggregate size-fractions. Adopting notillage and tree-based systems (such as the rubber tree plantation) would compensate the negative conversioneffect in the amount of organic matter and promote C and N storage mostly in the soil aggregate size-fractions.The effect of land-use conversions was more evident in the aggregates than in the whole soil, regardless of thesoil order. The conversions in both soil orders induced macroaggregate turnover and increased the yield ofnew free microaggregates.

© 2019 Elsevier B.V. All rights reserved.

Keywords:CacaoRubber treeSoil aggregatesFraction-size classesUltisolsAlfisols

1. Introduction

Climate change is a prominent sign of human-driven changes to theglobal environment and requires concentrated action tomitigate green-house gas emissions and reduce global warming. The Conference of theParties to theUnitedNations Framework Convention onClimate Changein Paris (November 30 to December 11, 2015) produced the Paris Cli-mate Agreement, a settlement to reduce climate change, limiting globalwarming to b2 degrees Celsius (°C) and to pursue efforts to limit the in-crease to 1.5 °C. As a result of this Conference, an initiative called 4 permil (4‰) was launched, an average sequestration rate to offset emis-sions of 0.6 t of C per hectare per year, with an aspiration to increase

ry, Av. Alberto Lamego 2000,

es).

global soil organic matter stocks by 4 per 1000 (or 0.4%) per year ascompensation for the global emissions of greenhouse gases by anthro-pogenic sources (Minasny et al., 2017; Ademe, 2015; Steffen et al.,2011). Soils are considered an asset in strategies for mitigating climatechange and there also exists the technical potential of agriculture tomit-igate CO2 (5.5–6.0 Gt CO2-Eq. yr−1) whose C sequestration in soil is re-sponsible for almost 89%, and therefore agriculture practices certainlycan and should be part of the solution to climate change (Minasnyet al., 2017; Ademe, 2015; Steffen et al., 2011; Smith et al., 2007).

Brazil's nationally determined contribution (NDC) includes a reduc-tion of its greenhouse gas emissions by 37% by 2025, with a further tar-get of a 43% reduction by 2030 (both compared to 2005 levels). Theactions required to implement the mitigation contribution outlined inthe NDC are to restore 15 million hectares of degraded pastures, aswell as implement an integrated crop livestock-forest system in 5 mil-lion hectares; to achieve zero illegal deforestation in the Amazon by

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2030, and to restore and reforest 12 million hectares of forests (http://www.mma.gov.br/clima/convencao-das-nacoes-unidas/acordo-de-paris, accessed August 27, 2018).

Therefore, it is imperative to adopt sustainable soil managementtechniques, which are so widely studied by soil science yet very littleimplemented in large-scale production systems. Agroforestry systemsand forestry systems are sustainable land-use systems which may playan important role in storing carbon aboveground and belowgroundthrough continuous deposition of plant residues, and also can be a strat-egy to restore degraded lands (Nair et al., 2010).

Cacao (Theobroma cacao L.) AFS, with around 711,850 ha planted inBrazil, are a combination of cacao trees with non-woody species (Musaparadisiaca, Manihot esculenta, etc.) and woody species (Erythrina,Gliricidia sepium,Hevea brasiliensis, etc.), whether in the formof second-ary forest (cabruca) or under homogeneous forest. These systems offerevidence of compatibility and complementarity of different species,and at the same time demonstrate the sustainability of multi-layeredproduction systems (Müller and Gama-Rodrigues, 2012; Nair et al.,2009). (The next paragraph was removed) Cacao AFS may play an im-portant role in the sequestration of soil organic carbon (SOC) and totalsoil N (TSN) through continuous deposition of plant residue. The largeamounts of leaf litter, roots and woody material from shade species aswell as cacao represent a substantial addition of C into these systems,most of which is stored in the soil both on the surface and in depthafter decomposition (Monroe et al., 2016; Fontes et al., 2014; Albrechtand Kandji, 2003). The average C content stored in soil (0–50 cm) incacao AFSs is approximately 83 Mg ha−1 (Fontes et al., 2014) and inthe range of 100–300 Mg ha−1 to 1 m depth (Monroe et al., 2016;Mattos, 2016; Gama-Rodrigues et al., 2010). Articles regarding TSN indepth are scarce, especially in soils under AFSs. Gelaw et al. (2014)found TSN stock around 3 Mg ha−1 in AFSs with Faidherbia albida andaround 4 Mg ha−1 in silvopasture systems also with Faidherbia albidaup to 30 cm depth. Kassa et al. (2017) found TSN stock up to 60 cmdepth in the range of 36 to 45 Mg ha−1 in soils under different AFSs.(The next paragraph was removed).

In Brazil, reforestation with rubber trees has spread all over thecountry with a planted area of around 170 thousand ha (AssociaçãoBrasileira de Produtores de Florestas Plantadas – ABRAF, 2013;Wauters et al., 2008). Some studies have shown the potential of soil or-ganic C (SOC) stock in rubber tree plantations in Brazil (55.2 to105.5 Mg ha−1 at depth 0–60 cm) (Maggiotto et al., 2014; Wauterset al., 2008). However, the SOC stock may be higher than 200 Mg ha−1

in agroforestry or forestry systems up to 100 cm depth (Vicente et al.,2016; Monroe et al., 2016; Salgado et al., in press).

In addition, studies on cacao-producing areas in the south ofBahia, Brazil, showing the effect of secondary forest conversion topasture, rubber tree plantations or agroforestry systems are scarce,and the few which have been carried out show that changes in SOCstock can increase, decrease or not even alter the accumulatedvalues. For example, Monroe et al. (2016) showed that the conver-sion of secondary forest to 4-year-old cacao and rubber AFS werethe most efficient in accumulating SOC in the top 20 cm of the soil,and the conversion of secondary forest to cacao AFS older than20 years were similar to the natural forest regarding the accumula-tion of SOC along the soil profile. In turn, Mattos et al. (in press)showed that after the conversion of secondary forest into pasturethe SOC stock was similar in both systems. On the other hand, theyalso showed that the conversion of secondary forest into a rubbertree plantation increased the SOC stock, and the conversion of sec-ondary forest into agroforestry systems (rubber tree and açai AFSand rubber tree and cacao AFS) decreased the SOC stock up to100 cm. Therefore, one general question remains unclear: Couldthe effect of secondary forest conversion into pasture or rubbertree plantation and cacao + erythrina AFS conversion into cacao+rubber tree AFS on the C and N storage in soils and aggregate-size fractions be compensated by a high amount of organic residues

deposited over the years by rubber tree plantation and agroforestrysystems (above and belowground) and a high amount of below-ground residues deposited by pasture?

Another important issue related to soil C sequestration is the or-ganic matter stored in subsurface horizons, as it represents high pro-portions of C of around 46% to 63% which is stored in the first meterof soils worldwide, mainly in tree-based production systems(Vicente et al., 2016; Ademe, 2015; Rumpel and Kögel-Knabner,2011). The distribution of TSN within the soil profile showed a sim-ilar pattern of organic soil C, i.e. it reduces from the surface towardsthe subsoil and reaches stability in deeper soil horizons (Song et al.,2016). Hence, the relevance of studying C and N stock up to 1-meter-deep in these soils is categorical.

There is consensus in the literature regarding a link between SOCstock in agroforestry and forestry systems and soil aggregation due tothe continuous addition of plant residues coupled with the absence oftillage. The formation of aggregates in natural and/or no tillage systemsis due to plant residue decomposition, which forms coarse intra-aggregate particulate organic matter, later transformed by microorgan-ism action into fine intra-aggregate particulate organic matter (fineiPOM). This process happens inside soil macroaggregates. This fineiPOMbecomes embedded in clay minerals and inmicrobial compoundsover time, consequently forming microaggregates within macroaggre-gates. Gama-Rodrigues et al. (2011 and 2010) suggest that no-till andthe continuous supply of organic matter through cacao AFSs favor ag-gregation, and therefore macroaggregation would be the main mecha-nism of C stabilization in these soils.

Considering the above, the objective of the present study was toevaluate the carbon and nitrogen stocks in soils and in the differentsoil aggregate-size fractions up to 1 m between different land-use sys-tems in two soil orders in the south of Bahia, Brazil.

2. Materials and methods

2.1. Characterization of the study area

Soil samples were collected from sites located in the municipality ofUna, (15°16′ 11″ S, 39° 4′ 10″ W) and in the Cocoa Research Center(CEPEC/CEPLAC) in the municipality of Ilhéus (14°47′ 50′ S and 39°2′8′ W). All the sites are located in the southern region of the state ofBahia. The region's climate is Af according to the Köppen classification,and the mean annual rainfall is around 1647 mm, with mean annualtemperature around 24.3 °C.

Prior to the installation of the production systems, the original veg-etation cover was secondary forest, which was felled, dismantled witha track tractor and then plowed andharrowed. The studywas composedof five different land use systems, namely: (1) cacao (Theobroma cacaoL.) + rubber tree (Hevea brasiliensis Muell. Arg.) AFS, 12 years of age,cacao row spacing was in four rows of 2 × 2.5 m. Lines L1 and L4 wereplanted at a distance of 2.5 m from the hevea hedgerows. Doublehevea hedgerows at a density of 7 × 4 × 3 m, without inorganic fertili-zation since 2006; (2) cacao + erythrina (Erythrina glauca Lour.) AFS,35 years of age, erythrina spacing of 25 × 25 m, distributed in a quin-cunx that totaled 32 trees per hectare, while cacao tree spacing was 3× 3 m, without inorganic fertilization since 1990; (3) rubber tree plan-tation, 35 years of age, spacing 7 × 3m,without fertilization since 1982,and presence of grass as cover; (4) unfertilized pasture formed byBrachiaria decumbens, 30 years of age; (5) an Atlantic Forest fragmentas secondary forest.

The soils of the rubber tree plantation, pasture and secondary forest(SF) sites are classified as Dystrophic Yellow Argisols (Ultisols) and Eu-trophic Haplic Nitosols (Alfisols) for the sites of cacao+ rubber tree andcacao + erythrina AFSs. In the Nitosols there were no secondary forestor pasture sites next to the AFS sites. In this case, we consider thecacao+ erythrina AFS as the reference system, since it is the oldest sys-tem andwaswidely adopted in the region. Erythrina has currently been

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replaced by rubber trees due to its economic value and rapid growth(Monroe et al., 2016).

2.2. Soil sampling

Four uniform (in terms of soil homogeneity, slope, historical land-use, density and tree age) fixed plots (30 × 30 m) were delimited inthe central part of each land use system and separated by at least100 m. Trenches (1 × 1 × 1.5 m) were opened between plant rows ineach plot, and soil was collected at six depths (0–10, 10–20, 20–40,40–60, 60–80 and 80–100 cm). The soil samples from each depthwere air-dried and passed through a 2mmsieve, then particle size anal-ysis was performed by the pipette method, and the volumetric ringmethod was used to determine soil density (Table 1) (Embrapa.Embrapa Solos, 2017). Soil organic carbon (SOC) and total soil nitrogen(TSN) was determined by dry combustion in an automated elementalanalyzer system (CHNS/O analyzer), while the bulk density of eachsoil depth was used to calculate the amount of SOC and TSN stored at1mdepth and expressed asMg ha−1. The SOC (and TSN) stockwas sub-sequently corrected according to the thickness of each soil layer, consid-ering the secondary forest (for Argisols) and cacao+ erythrina AFS (forNitosols) soil layers as the reference thickness. This correction is recom-mended due to the influence of the soil layer in calculating SOC/TSNstock, which was done according to the following formula:

Dad=sub ¼ Mref :–Mtrat:ð Þ=BD

100

In which: Dad/sub= depth to be added or subtracted in the stock cal-culation (cm); Mref. = soil mass at the reference soil depth (Mg ha−1);Mtrat. = soil mass at the treatment soil depth (Mg ha−1); and BD = soilbulk density (g/cm−3).

Table 1Particle size fractions and soil bulk density (SBD), up to 100 cm, innatural forest, grassland,rubber tree plantation and different cacao AFS in the Southern Bahia. Brazil.

Depth(cm)

Particle sizefraction (%)andbulk density(gcm−3)

Naturalforest

Pasture RubbertreePlantation

Cacao+rubbertree

Cacao +erythrina

0–10 Sand 88.95 93.26 85.31 24.71 14.44Silt 0.81 2.41 3.05 25.32 26.71Clay 10.25 4.33 11.64 49.97 58.85SBD 1.31 1.31 1.31 1.06 1.06

10–20 Sand 82.61 93.01 80.18 21.66 14.50Silt 1.89 2.36 4.04 26.03 23.68Clay 15.51 4.63 15.78 52.31 61.82SBD 1.49 1.49 1.49 1.01 1.01

20–40 Sand 74.10 87.98 73.95 27.22 10.59Silt 1.70 3.34 4.45 22.91 23.89Clay 24.20 8.68 21.60 49.88 65.52SBD 1.50 1.50 1.50 1.10 1.10

40–60 Sand 64.77 75.33 70.15 14.29 8.20Silt 3.38 1.47 3.83 20.85 17.08Clay 31.85 23.20 26.01 64.86 74.72SBD 1.47 1.47 1.47 0.90 0.90

60–80 Sand 59.25 69.96 70.73 11.78 8.03Silt 6.40 3.37 4.02 17.78 17.34Clay 34.35 26.67 25.26 70.43 74.62SBD 1.48 1.48 1.48 1.02 1.02

80–100 Sand 60.78 69.31 69.29 15.94 7.72Silt 1.35 3.55 3.83 20.40 32.12Clay 37.86 27.14 26.88 63.66 60.16SBD 1.40 1.40 1.40 1.02 1.02

2.3. Fraction-size separation

Theprocedure consisted inweighing100 g dry soil, passed through a2000 μmsieve and submerged in a 500-ml beaker of deionizedwater foraboutfive-minute before placing it on top of a 250-μmsieve. The sievingwas done manually, moving the sieve up and down about 3 cm, 50times, for 2 min. The entire fraction remaining at the top of the250-μm sieve was collected in hard plastic pans. The fraction thatwent through the sieve (b250 μm) was then passed through a 53-μmsieve, which separated this material into two new fractions by thesame previous sieving procedure. Three aggregate size classes were ob-tained: macroaggregates (2000–250 μm), microaggregates (250–53μm), and the silt + clay fraction (b53 μm). All fractions were dried ina forced-circulation air oven at 60 °C for 72 h, and the weight percent-ages of each fraction were subsequently calculated (Elliot, 1986;Gama-Rodrigues et al., 2010). The overall average recovery mass per-centage of soil fractions after the wet-sieving procedure was about98% of the initial soil mass.

The SOC and TSN in aggregate size classes was also determined bydry combustion in an automated elemental analyzer system (CHNS/Oanalyzer). The C and N storage in aggregate size classes was calculatedbymultiplying the C concentration (or N concentration) (g/kg soil in ag-gregate size) with soil bulk density of depth interval (kg/m−3) and theweight percentage of the fraction.

2.4. Statistical analyzes

Data were tested for normality by the Kolmogorov-Smirnov andLilliefors methods to evaluate the normal distribution of the analyzedvariables, as well as homoscedasticity and normal distribution residues.Thus, the data that did not present normality were transformed by theequations arcsen√Xi /100 and log. The data were subjected to principalcomponent analysis (PCA) to evaluate the degree of dissimilarity be-tween the assessed sites considering the soil orders. PCA enabled clus-tering the sites evaluated in diagrams which consider the data setsimilarity of the variables along the ordination axes. We considered avector load b0.70 to be a low correlation for interpreting the principalcomponents. Two components considered significant were obtainedbased on the PCA, and these components facilitate interpreting thebidimensional plots. The direction and length of arrows show the corre-lation quality between the variables, and between the variables andprincipal components (axis X and Y). The arrows with narrow anglesare strongly correlated, while arrows that are perpendicular show nocorrelation (Viana et al., 2018; Aleixo et al., 2017; Fontes et al., 2014;Gomes et al., 2004).

3. Results

3.1. Soil organic C (SOC) and total soil N (TSN) stocks in depth

In the Argisols, the SOC stored in pasture and in the rubber planta-tion was approximately 11 and 15% lower than in secondary forest, re-spectively. The average SOC stock in the rubber tree plantation wasalmost 5% lower than pasture (Fig. 1). The TSN stock in the pasturewas only 2% higher than in the secondary forest; in turn, the TSNstock in the rubber tree plantation was approximately 70% lower thanin the secondary forest and in the pasture (Fig. 2). In the Nitosols, thedifference in SOC stock between the AFSs was approximately 4%, andthe greatest value was in the cacao + erythrina AFS. The TSN stockwas 46% higher in the cacao + rubber AFS up to 100 cm of depth(Figs. 1 and 2).

The secondary forest and the rubber tree plantation showed an in-crease in the SOC stock up to 40 cm depth and the pasture up to thefirst 60 cm. There was a decrease along the profile from these depths.The cacao + erythrina AFS stood out from the cacao + rubber treeAFS, accumulating around 50% more SOC in the first 20 cm of soil.

Fig. 1. Soil organic carbon stocks in the 0–100 cm soil layer in natural forest, pasture,rubber tree plantation on Argisols and different cacao AFS on Nitosols in the SouthernBahia, Brazil. Vertical bars represent ± standard error. SF: secondary forest; PAS: pasture;RT: rubber tree plantation; C + RT: cacao and rubber tree agroforestry system; C + E:cacao and erytrina agroforestry system.

Fig. 3. SOC stocks at different dephts of soil under natural forest, pasture, rubber treeplantation on Argisols and different cacao AFS on Nitosols in the Southern Bahia, Brazil.Vertical bars represent ± standard error. SF: secondary forest; PAS: pasture; RT: rubbertree plantation; C + RT: cacao and rubber tree agroforestry system; C + E: cacao anderytrina agroforestry system.

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The C stock decreased along the soil profile below this depth in bothAFSs. Regarding TSN stock, the secondary forest, pasture and the AFSspresented values almost two times higher below 20 cm than in thegreater depths. On the other hand, the rubber tree plantation presentedsimilar TSN values accumulated along the soil profile (Figs. 3 and 4).

3.2. Depth-wise distribution of soil size fractions and their SOC and TSN

In the Argisols, the macro-size fraction was predominant in alldepths, followed by micro-size fraction and silt + clay fraction in allland-uses. On the other hand, Nitosols under the AFSs (which presentedhigher clay content) presented the smallest amounts ofmacro-size frac-tion and the greatest amount of silt + clay fraction along the soil profile.In general, the amount of macro-size fraction decreased and the micro-size fraction increased along the soil profile in all land-use systems.The silt + clay fraction also increased along the soil profile, but only intheArgisol order. The amount ofmicroaggregateswas higher in the pas-ture and in the rubber tree plantation,while the amount ofmacroaggre-gates was higher in SF. The amount of macroaggregates and silt + clayfraction varied little between AFSs, but the amount of microaggregates

Fig. 2. Total N stocks in the 0–100 cm soil layer in natural forest, pasture, rubber treeplantation on Argisols and different cacao AFS on Nitosols in the Southern Bahia, Brazil.Vertical bars represent ± standard error. SF: secondary forest; PAS: pasture; RT: rubbertree plantation; C + RT: cacao and rubber tree agroforestry system; C + E: cacao anderytrina agroforestry system.

Fig. 4. Total N stock at different dephts of soil under natural forest, pasture, rubber treeplantation on Argisols and different cacao AFS on Nitosols in the Southern Bahia, Brazil.Vertical bars represent ± standard error. SF: secondary forest; PAS: pasture; RT: rubbertree plantation; C + RT: cacao and rubber tree agroforestry system; C + E: cacao anderytrina agroforestry system.

Fig. 5. Depthwise distribution of three soil size fractions under natural forest, pasture, rubber tree plantation and different cacao AFS in Southern Bahia, Brazil. Vertical bars represent ±standard error. SF: secondary forest; PAS: pasture; RT: rubber tree plantation; C + RT: cacao and rubber tree agroforestry system; C + E: cacao and erytrina agroforestry system.

5C.V. Oliveira et al. / Geoderma Regional xxx (2019) e00218

was N30% higher in the cacao + rubber tree AFS up to 40 cm and thesedifferences decreased below this depth (Fig. 5).

C stock in the macro-size fraction of soil under the pasture up to100 cm depth was approximately 50% lower than the secondary forestand the rubber tree plantation. Equally, the difference in C stock up to20 cm between the AFSs in the macro-size fraction was 50%, with thehighest values in the cacao + erythrina AFS. In relation to the micro-size fraction, C stock in the secondary forest and pasture were 40 and24% lower, respectively, than the rubber tree plantation up to 100 cmdepth. On the other hand, the AFSs presented very similar amounts ofC stock in the micro-size fraction. The C stock in the pasture in the silt+ clay fraction from 20 cm was approximately 30% higher than in thesecondary forest and in the rubber tree plantation. Meanwhile, the dif-ference among AFSs was approximately 10%. It is worth noting thatAFSs presented larger C stocks in the silt + clay fraction (Fig. 6).

The N stock in macro-size fraction up to 100 cm of depth in the rub-ber tree plantation was almost two-times larger when compared tothe secondary forest and pasture; and the difference between them inthe AFSs (Nitosols) was around 30%. The rubber tree plantation kept

the largest N stock in the micro-size fraction up to 100 cm, which waspractically twice greater than the value observed for the pasture and75% greater than the secondary forest. The AFSs were quite similarto each other in terms of TSN stock in the micro-size fraction. The TSNstock of the silt + clay fraction was practically the same in thesecondary forest, pasture and rubber plantation, as well as betweenthe AFSs (Fig. 7).

3.3. Principal components analysis

The C andN storage in the soil and in the different soil aggregates areassociated with two main components (PC1 explained 61.86% and PC2explained 18.70%) (Fig. 8), and the ordination diagram shows theNitosols on the left side and theArgisols on the right side of the diagram.The pasture and the secondary forest are located on the right side of thelower quadrant and formed two different groups, while cacao +erythrina AFS (located in the upper quadrant) and cacao + rubbertree AFS (located in the lower quadrant) are located on the left side ofthediagramand formed one group. The rubber tree plantation is located

Fig. 6.Depthwise distribution of organic carbon stocks in different soil size fractions under secondary forest, pasture, rubber tree plantation on Argisols and different cacao AFS onNitosolsin the Southern of Bahia, Brazil. Vertical bars represent± standard error. SF: secondary forest; PAS: pasture; RT: rubber tree plantation; C+RT: cacao and rubber tree agroforestry system;C + E: cacao and erytrina agroforestry system.

6 C.V. Oliveira et al. / Geoderma Regional xxx (2019) e00218

on the right side of the upper quadrant and represents another group(Fig. 8). The variables which are more closely associated with PC1and thus more discriminant in forming the heterogeneous groups(load N0.70) are C and N from different soil-size fractions, while SOCand TSN stock are associated with PC2 (Fig. 8).

4. Discussion

As expected, C andN stock in soils and in the different soil aggregate-size fractions revealed that the dissimilarity between sites was stronglyinfluenced by soil order. There was high dissimilarity between the sitesin Nitosols and those in Yellow Argisols, and the dissimilarity betweenthe land use systems only occurred in the Yellow Argisol (Fig. 8). Ourresults reinforce previous studies which show that the conversion ofsecondary forest into pasture and/or forest systems or between agrofor-estry systems can provide changes in SOC and TSN stock, increasing ordecreasing it, or not even alter the accumulated values (Rittl et al.,2017; Guo and Gifford, 2002; Cerri et al., 2004). For example, Vicente

et al. (2016) observed that the conversion of secondary forest into rub-ber tree plantation increased SOC stock by 46 Mg ha−1 up to 100 cm.Rubber tree plantations can act as a carbon sink by sequestering carbonin biomass and in soils. According to Wauters et al. (2008), the SOCstock (0–60 cm) in a 14-year-old rubber tree plantation was 153 Mg Cha−1. Although these conversions did not result in a significant decreasein SOC stock, we should not neglect the importance of forests in accu-mulating organic matter, and therefore in C sequestration within thesoil-plant-atmosphere system, as well as the possibility of CO2 emissionto the atmosphere during the conversion process of secondary forestinto pasture and/or forest system,mainly in the first years after the con-version. In the present studywe cannot affirmwhether or not therewasa reduction in SOC and TSN stock in the first years after the conversion,but we observed that both pasture and rubber tree plantation storedequivalent amounts of SOC to the secondary forest after 30 years. Thereduction in the TSN stockwith the introduction of the rubber tree plan-tation up to 100 cm is noticeable. Some articles in the literature rein-force the results of the present study that the conversion of secondary

Fig. 7.Depthwise distribution ofN stocks in different soil size fractions under natural forest, pastured, rubber tree plantation onArgisols and different cacao AFS onNitosols in the Southernof Bahia, Brazil. Vertical bars represent ± standard error. SF: secondary forest; PAS: pasture; RT: rubber tree plantation; C + RT: cacao and rubber tree agroforestry system; C + E: cacaoand erytrina agroforestry system.

7C.V. Oliveira et al. / Geoderma Regional xxx (2019) e00218

forest into rubber plantation reduces TSN stock (De Blécourt et al., 2013;Yang et al., 2004).

In the Nitosols, the PCA showed that there was no dissimilarityamong the AFSs, probably because the conversion effect was restrictedto the surface soil (Fig. 8). As such, 12 years of conversion could nothave been enough to produce larger changes in SOC stock along the pro-file, as occurred for the conversions in the Argisols. Therewas also an in-crease of almost two-fold in the TSN stock up to 100 cmafter 12 years oferythrina replacement by the rubber tree in the AFS (Figs. 1 and2).Moststudies have shown that the use of leguminous plants increases the TSNstock due to their inherent ability to fix the atmospheric nitrogen by theassociation with symbiotic bacteria (Jia et al., 2012; Sharrow and Ismail,2004). In turn, other studies have shown that rubber-based agroforestrysystems increase both SOC and TSN stock (Chen et al., 2017; Fox et al.,2014). In the present study, the cacao + erythrina AFS at the age of35 years is characterized as a mature system that presents a stableand slow growth rate, and consequently low accumulation of vegetalresidues and reduced root cycling. These factors contribute to the Ntransformation in plant residues occurring more slowly and gradually.

On the other hand, younger agroforestry systems and/or forest planta-tions present a high growth rate and high rates of organic matter accu-mulation, root cycling and exudate production by trees. Therefore, theymay present high accumulation rates of C andN in soil, often accumulat-ing higher or similar amounts to the secondary forest rates (Kassa et al.,2017). Monroe et al. (2016) investigated soils under different cacao AFSin southern Bahia and observed that 4-year-old cacao+ rubber tree AFShad a higher C stock up to 100 cmdepth than the older cacao AFS (above20 years of age).

Both soil classes under similar edaphic conditions and land use sys-tems with significant input of organic residues showed similar results:the average SOC stock in Acrisols was 207 Mg ha−1 up to 100 cmdepth, and 72 Mg ha−1 was stored at the first 30 cm depth; while theaverage SOC stock in Nitosols was 224 Mg ha−1 up to 100 cm, and116Mg ha−1 at 30 cmdepth. However, these same soils classes showeda reduction in the average of SOC stock under different climatic condi-tions and land use systems with low input of plant residues. For exam-ple, while Santana et al. (2019) found SOC stock of around 80 Mg ha−1

up to 100 cm under pasture and agriculture, Zanatta et al. (2007) found

Fig. 8.Ordination diagram produced by principal component analysis of C and N storage in the soil and in the different soil aggregates. SF: secondary forest; RT P: rubber tree plantation; C+ RT AFS: cacao + rubber tree agroforestry system; C + E AFS: cacao + erythrina agroforestry system. The AFSs are on Eutrophic Haplic Nitosols and the other sites are on DystrophicYellow Argisols.

8 C.V. Oliveira et al. / Geoderma Regional xxx (2019) e00218

approximately 60 Mg ha−1 for grassland in Acrisols at 30 cm depth.Batjes (2005) found 61 and 103 Mg ha−1 of SOC stock in Nitosols at30 cm and up to 100 cm depth, respectively. These results emphasizethe relevance of high input of organic residues (above and below-ground) from forestry and agroforestry systems on the enhancementof carbon content in these soils.

The macro-size soil fraction was predominant in the secondary for-est, pasture and the rubber tree plantation at all depths. This larger frac-tion decreased while the silt + clay fraction increased with depth. Incontrast, the silt + clay fraction in soils under the AFSs was superiorto the aggregate classes. Tonucci et al. (2011) and Gama-Rodrigueset al. (2010) also found similar results for themacro-size fraction; how-ever, these authors did not find any variation of the silt + clay fractionalong the soil profile. The silt+ clay fraction is closely related to soil par-ticle size, and therefore directly influenced by the percentage of claycontent of each soil, and which explains the higher amount of silt+ clay fraction in the soils under AFSs (Table 1). Themacro-size fractiondecreased and themicro-size fraction increasedwith all the conversionsup to 1 m in the Argisols and up to 20 cm in the Nitosols (Fig. 5). Addi-tionally, the conversion to rubber tree plantation kept the C levels sim-ilar to the secondary forest, while the conversion of secondary forestinto pasture reduced the C stock in the macro-size fraction (Fig. 6).These results suggest the initial C loss for pasture establishment mighthave been considerably higher than that for the rubber tree plantation.First, this result was due to inadequate pasture management, meaningthe reduction in vegetable biomass caused by continuous grazing with-out restoring vegetal biomass by soil fertilization, thereby compromis-ing the C accumulation in the macro-size fraction. Second, thisreduction in plant biomass due to the lack of fertilization may have af-fected the microbial activity in the soil under pasture, which meansthe lower plant material input reduced substrate availability for micro-biota, in turn favoring C mineralization bound to the macro-size frac-tion. Moreover, the tree-based systems (such as the rubber treeplantation) would compensate the negative conversion effect in theamount of C in both soil and macroaggregates through continuousdeposition of plant residues.

On the other hand, those conversions increased C stock in themicro-size fraction along the soil profile. In relation to N, the conversion ofsecondary forest to pasture did not change N stock in the macro-sizefraction, while it increased in the micro-size fraction, and almost didnot change in the silt+ clay fraction up to 1m.However, N in the rubbertree plantation increased twice its value in relation to the secondary for-est in the macro and micro-size fractions, while the N stock in the silt+ clay fraction was similar to the other systems along the soil profile(Figs. 6 and 7).

In the Argisols, the conversion of forest to rubber tree plantationwasmore efficient in keeping C and N in the macro-size fraction up to 1 m.The macro-size fraction is generally the fraction which most stocks Cand N, mainly in systems with high plant residue inputs (Lenkaand Lal, 2013) such as rubber tree plantations. Macroaggregates areformed around fresh residues because they are a source of C and N formicrobial activity and for the production of microbial-derived bindingagents such as fungal hyphae, fine roots, hyphae (particularlyvesicular-arbuscular mycorrhizal hyphae) and microbial products,which can persist for months or years, depending on soil management(Six and Paustian, 2014).

The dissimilarity between the land use systems shown by the PCA inthe Argisols suggests that soil tillage during the conversion of forest topasture and also the conversion of forest into rubber tree plantationpromoted a breakdown of the macroaggregates, and consequently therelease of free microaggregates and C and N mineralization whichwere protected in the larger fraction (Six et al., 2004). Thus, the highestC and N values in the micro-size fraction of soils under pasture and therubber tree plantation suggest that the increases in macroaggregateturnover induced by tillage after these conversions yields fewer newfree microaggregates and an incorporation of new C and N into freemicroaggregates over time, since there was no more soil disturbance.However, the 12-year replacement of shading trees in the Nitosolswas not enough to enable incorporation of new C and N into the freemicroaggregates. In addition, the conversion of cacao + erythrina AFSinto cacao + rubber tree AFS reduced almost half of the C and N stockin the macro-size fraction up to 20 cm. These results suggest that soil

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disturbance induces a loss of C-rich macroaggregates and a gain in C-depleted microaggregates (Six et al., 2000).

5. Conclusions

Adopting no tillage and tree-based systems (such as the rubbertree plantation) would compensate the negative conversion effectin the amount of organic matter and promote C and N storage mostlyin the soil aggregate size-fractions.

The effect of land-use conversions was more evident in the aggre-gates than in thewhole soil, regardless of the soil order. The conversionsin both soil orders induced macroaggregate turnover and increased theyield of new free microaggregates. However, only the forest conversioninto pasture and the forest conversion into rubber tree plantation en-abled incorporating and consequently physically protecting new C andN into the micro-size fraction.

The conversion effect of cacao + erythrina AFS into cacao + rubbertree AFS was restricted to the surface soil and did not promote dissimi-larity among the AFSs regarding the C and N storage in the whole soiland aggregate size-fractions. Additionally, 12 years of conversion wasnot enough to promote new C and N incorporation into the new freemicroaggregates yield after the macroaggregate turnover induced bytillage during this conversion.

Acknowledgments

We thankCAPES for granting amaster science scholarship to thefirstauthor. This researchwas partially supported by a grant of Brazilian Na-tional Council for Scientific and Technological Development (CNPq)(302842/2014-4). We are grateful to Kátia R. Nascimento Sales,Ederaldo Azeredo Silva and Vanilda Ribeiro de Souza of Soil Laboratory,North Fluminense State University for technical support in soil samplecollection and analysis.

Appendix A. Supplementary data

Supplementary data associated with this article can be found in theonline version, at doi: https://doi.org/10.1016/j.geodrs.2019.e00218.These data include the Google maps of the most important areasdescribed in this article.

References

Ademe, 2015. Organic carbon in soils. Meeting Climate Change and Food Security Chal-lenges. ADEME, France.

Albrecht, A., Kandji, S.T., 2003. Carbon sequestration in tropical agroforestry systems.Agric. Ecosyst. Environ. 99, 15–27.

Aleixo, S., Gama-Rodrigues, A.C., Costa, M.G., Sales, M.V.S., Gama-Rodrigues, E.F., Marques,J.R.B., 2017. P transformations in cacao agroforests soils in the Atlantic forest region ofBahia, Brazil. Agrofor. Syst. 91, 423–437.

Associação Brasileira de Produtores de Florestas Plantadas – ABRAF, 2013. Anuárioestatístico 2013, ano base 2012. DF, Brasília, p. 148 (ISSN 1980-8550).

Batjes, N.H., 2005. Organic carbon stocks in the soils of Brazil. Soil Use Manag. 21, 22–24.Cerri, C.E., Paustian, K., Bernoux, M., Victoria, R.L., Melillo, J.M., Cerri, C.C., 2004. Modeling

changes in soil organic matter in Amazon forest to pasture conversion with the cen-tury model. Glob. Chang. Biol. 10, 815–832.

Chen, C., Liu, W., Jiang, X., Wu, J., 2017. Effects of rubber-based agroforestry systems onsoil aggregation and associated soil organic carbon: implications for land use.Geoderma 299, 13–24.

De Blécourt, M., Brumme, R., Xu, J., Corre, M.D., Veldkamp, E., 2013. Soil carbon stocks de-crease following conversion of secondary forests to rubber (Hevea brasiliensis) plan-tations. PLoS ONE 8, e69357.

Elliot, E.T., 1986. Aggregate strucuture and carbon, nitrogen and phosphorus in native andcultivated soils. Soil Sci. Soc. Am. J. 50, 627–633.

Embrapa. Embrapa Solos, 2017. Manual de Métodos de Análise de Solos. 3nd ed. DF,Brasília, p. 573 rev.

Fontes, A.G., Gama-Rodrigues, A.C., Gama-Rodrigues, E.F., Sales, M.V.S., Costa, M.G.,Machado, R.C.R., 2014. Nutrient stocks in litterfall and litter in cocoa agroforests inBrazil. Plant Soil 383, 313–335.

Fox, J., Castella, J.C., Ziegler, A.D., 2014. Swidden, rubber and carbon: can REDD+work forpeople and the environment in Montane Mainland Southeast Asia? Glob. Environ.Chang. 29, 318–326.

Gama-Rodrigues, E.F., Nair, P.K.R., Nair, V.D., Gama-Rodrigues, A.C., Baligar, V.C., Machado,R.C.R., 2010. Carbon storage in soil size fractions under two cacao agroforestry sys-tems in Bahia, Brazil. Environ. Manag. 45, 274–283.

Gama-Rodrigues, E.F., Gama-Rodrigues, A.C., Nair, P.K.R., 2011. Soil carbon sequestrationin cacao agroforestry systems: A case study from Bahia, Brazil. In: Kumar, B.M.,Nair, P.K.R. (Eds.), Carbon Sequestration Potential of Agroforestry Systems. Advancesin Agroforestry 8. Springer, New York, pp. 85–99.

Gelaw, A.M., Singh, B.R., Lal, R., 2014. Soil organic carbon and total nitrogen stocks underdifferent land usesin a semi-arid watershed in Tigray, Northern Ethiopia. Agric.Ecosyst. Environ. 188, 256–263.

Gomes, J.B.V., Curi, N., Motta, P.E.F., Ker, J.C., Marques, J.J.G.S.M., Schulze, D.G., 2004. Prin-cipal component analysis of physical, chemical, and mineralogical attributes of thecerrado biome soils. Rev. Bras. Ci. Solo 28, 137–154.

Guo, L.B., Gifford, R.M., 2002. Soil carbon stocks and land use change: a meta-analysis.Glob. Chang. Biol. 8, 345–360.

Jia, X., Wei, X., Shao, M., Li, X., 2012. Distribution of soil carbon and nitrogen along arevegetational succession on the loess plateau of China. Catena 95, 160–168.

Kassa, H., Dondeyne, S., Poesen, J., Franll, A., Nyssen, J., 2017. Impact of deforestation onsoil fertility, soil carbon and nitrogen stocks: the case of the Gacheb catchment inthe White Nile Basin, Ethiopia. Agric. Ecosyst. Environ. 247, 273–282.

Lenka, N.K., Lal, R., 2013. Soil aggregation and greenhouse gas flux after 15 years of wheatstraw and fertilizer management in a no-till system. Soil Till. Research 126, 78–89.

Maggiotto, S.R., Oliveira, D., Marur, C.J., Stivari, S.M.S., Leclerc, M., Wagner- Riddley, C.,2014. Potential carbon sequestration in rubber tree plantations in the northwesternregion of the Paraná state, 549 Brazil. Acta Sci. Agron. 36, 239–245.

Mattos, G.S., 2016. Estoque de carbono orgânico do solo em sistemas agroflorestais comseringueira no sul do estado da Bahia, Brasil. Campos dos Goytacazes – RJ: UENF.Tese (Doutorado em Produção Vegetal)–Universidade Estadual do Norte FluminenseDarcy Ribeiro, p. 70.

Minasny, B., Malone, B.P., Mc Bratney, A.B., et al., 2017. Soil carbon 4 per mille. Geoderma292, 59–86.

Monroe, P.H.M., Gama-Rodrigues, E.F., Gama-Rodrigues, A.C., Marques, J.R.B., 2016. Soilcarbon stocks and origin under different cacao agroforestry systems in southernBahia, Brazil. Agric. Ecosyst. Environ. 221, 99–108.

Müller, M.W., Gama-Rodrigues, A.C., 2012. Cacao agroforestry systems. In: Valle, R.R.(Ed.), Science, Technology and Management of Cacao Tree. CEPLAC/CEPEC, Brasília,pp. 246–271.

Nair, P.K.R., Kumar, B.M., Nair, V.D., 2009. Agroforestry as a strategy for carbon sequestra-tion. J. Plant Nutr. Soil Sci. 172, 10–23.

Nair, P.K.R., Nair, V.D., Kumar, B.M., Showalter, J.M., 2010. Carbon sequestration in agro-forestry systems. Adv. Agron. 108, 237–307.

Rittl, T.F., Oliveira, D., Cerri, C.E.P., 2017. Soil carbon stock changes under different landuses in the Amazon. Geoderma Reg. 10, 138–143.

Rumpel, C., Kögel-Knabner, I., 2011. Deep soil organic matter—a key but poorly under-stood component of terrestrial C cycle. Plant Soil 338, 143–158.

Santana, M.S., Sampaio, E.V.S.B., Giongo, V., et al., 2019. Carbon and nitrogen stocks of soilsunder different land uses in Pernambuco state, Brazil. Geoderma Reg. 15, e00205.

Sharrow, S.H., Ismail, S., 2004. Carbon and nitrogen storage in agroforests, tree planta-tions, and pastures in western Oregon, USA. Agrofor. Syst. 60, 123–130.

Six, J., Paustian, K., 2014. Aggregate-associated soil organic matter as an ecosystem prop-erty and a measurement tool. Soil Biol. Biochem. 68, A4–A9.

Six, J., Elliot, E.T., Paustian, K., 2000. Soil macroaggregate turnover andmicroaggregate for-mation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol.Biochem. 32, 2099–2103.

Six, J., Bossuyt, H., Degryze, S., Denef, K., 2004. A history of research on the link between(micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res. 79,7–31.

Smith, P., et al., 2007. Policy and technological constraints to implementation of green-house gas mitigation options in agriculture. Agric. Ecosyst. Environ. 118, 6–28.

Song, B.L., Yan, M.J., Hou, H., Guan, J.H., Shi, W.Y., Li, G.Q., Du, S., 2016. Distribution of soilcarbon and nitrogen in two typical forests in the semiarid region of the loess plateau,China. Catena 143, 159–166.

Steffen, W., Persson, A., Deutsch, S., Zalasiewicz, J., et al., 2011. The Anthropocene: fromglobal change to planetary stewardship. Ambio 40, 739–761.

Tonucci, R.G., Nair, P.K.R., Nair, V.D., Garcia, R., Bernardino, F.S., 2011. Soil carbon storagein Silvopasture and related land-use Systems in the Brazilian Cerrado. J. Environ.Qual. 40, 825–832.

Viana, T.O., Gama-Rodrigues, A.C., Gama-Rodrigues, E.F., Aleixo, s., Moreira, R.V.S., Sales,M.V.S., Marques, J.R.B., 2018. Phosphorus transformations in alfisols and ultisolsunder different land uses in the Atlantic forest region of Brazil. Geoderma Reg. 14,e00184.

Vicente, L.C., Gama-Rodrigues, E.F., Gama-Rodrigues, A.C., 2016. Soil carbon stocks ofUltisols under different land use in the Atlantic rainforest zone of Brazil. GeodermaReg. 7, 330–337.

Wauters, J.B., Coudert, S., Grallien, E., JONARD, M., PONETTE, Q., 2008. Carbon stock in rub-ber tree plantations inWestern Ghana and Mato Grosso (Brazil). Forest. Ecol. Manag.255, 2347–2361.

www.mma.gov.br/clima/convencao-das-nacoes-unidas/acordo-de-paris (accessed Au-gust 27, 2018).

Yang, J.C., Huang, J.H., Pan, Q.M., Tang, J.W., Han, X.G., 2004. Long-term impacts of land-use change on dynamics of tropical soil carbon and nitrogen pools. J. Environ. Sci.China 16, 256–261.

Zanatta, J.A., Bayer, C., Dieckow, J., Vieira, F.C.B., Mielniczuk, J., 2007. Soil organic carbonaccumulation and carbon costs related to tillage, cropping systems and nitrogen fer-tilization in a subtropical Acrisol. Soil Tillage Res. 94, 510–519.