Soil & Tillage Research 205 (2021) 104785

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Soil & Tillage Research

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Soil carbon and nitrogen stocks and the quality of soil organic matter under T
silvopastoral systems in the Brazilian Cerrado
Luana Larrisa de Souza Almeidaa, Leidivan Almeida Frazãoa, Taynan Aquilles Marinho Lessaa,
Luiz Arnaldo Fernandesa, Álvaro Luiz de Carvalho Velosob, Angela Maria Quintão Lanac,
Igor Alexandre de Souzad, Rodinei Facco Pegoraroa, Evander Alves Ferreiraa,*
a
Instituto de Ciências Agrárias, Universidade Federal de Minas Gerais, Av. Universitária 1000, 39400-090, Montes Claros, MG, Brazil
b
Faculdades Integradas do Norte de Minas, Av. Osmane Barbosa 1111, 39404-006, Montes Claros, MG, Brazil
c
Escola de Veterinária, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, 31270-901, Belo Horizonte, MG, Brazil
d
Universidade Federal dos Vales do Jequitinhonha e Mucuri, Avenida Vereador João Narciso, 1380, 38610-000, Unaí, MG, Brazil

ARTICLE INFO ABSTRACT

Keywords: This study investigated soil carbon and nitrogen stocks and quality of soil organic matter in an Eutric Haplic
Carbon dioxide Cambisol four years after the conversion of degraded pastures into silvopastoral systems in the Brazilian Cerrado.
Humic factions The integrated production systems were composed of marandu grass (Urochloa brizanta) and Eucalyptus cloeziana
Integrated production systems or Eucalyptus urograndis. These systems were compared with areas of regenerating stratum and native vegetation
Soil microbial biomass
of the Cerrado biome. A randomized statistical design was used, and soil chemical and biological attributes and
soil CO2 efflux were evaluated (p < 0.05). After four years of implantation, soil carbon and nitrogen stocks
increased in silvopastoral systems in relation to regeneration stratum, but were still lower than those in native
vegetation. The chemical and granulometric soil fractionations indicated that carbon was protected in the most
stable soil organic matter fractions (humin and silt + clay). There was an increase in soil microbial carbon
during the rainy season and the metabolic quotient during the dry period. The deposition of plant material and
soil tillage in silvopastoral systems composed of marandu grass (Urochloa) and Eucalyptus cloeziana contributed
to an increase in soil microbial carbon at the 10–20 cm soil layer. The soil CO2 efflux, during the rainy and dry
seasons, was similar between both silvopastoral systems and native vegetation, probably indicating greater di-
versity of organisms and roots in these systems than in regeneration stratum. We conclude that the introduction
of integrated systems improved soil quality, allowing greater protection of soil organic matter.

1. Introduction successions of monocultures, contributing to the accumulation of C in

Integrated production systems are essential when the aim is sus-
tainable production, seeking to deal with the challenges of decades of
agricultural production with practices of high environmental impact.
Cited as models of low carbon (C) agriculture, these production systems
have been one of the precursors to the quality of Brazilian soils, and can
combine livestock, forestry, and crop activities in the same area,
practiced in rotation, succession, or intercropping (Rodrigues et al.,
2014). They allow the capture of CO2 in the soil through its removal
from atmospheric air, and thus make areas more productive and di-
versified, as far as agricultural production is concerned (Oliveira et al.,
2016).
The adoption of these production models contributes to the neu-
tralization of atmospheric C in previously occupied areas with
the soil, with rates that can reach ranges of 0.82–2.58 Mg ha−1 year−1.
Factors such as types of crops, edaphoclimatic conditions, and perma-
nence of the system in the area are determinant in the dynamics of C in
the soil (Carvalho et al., 2010). The interactions of raising animals with
annual crops and tree components may generate heterogeneity in nu-
trient availability and microbial activity throughout the system,
showing the complexity and need for more studies to evaluate these
systems (Guillot et al., 2019; Moraes et al., 2014; Oliveira et al., 2016).
In addition, the different kinds of vegetation that compose the
system contribute to the input of soil organic matter (SOM), supple-
menting the production of organic compounds of diverse chemical
nature that promote the increase and diversification of the soil micro-
biota (Oliveira et al., 2016). Also, the introduction of tropical grasses
into the integrated systems expands the entry pathways of readily

⁎
Corresponding author.
E-mail address: evanderalves@gmail.com (E.A. Ferreira).

https://doi.org/10.1016/j.still.2020.104785
Received 7 November 2019; Received in revised form 5 August 2020; Accepted 10 August 2020
Available online 01 September 2020
0167-1987/ © 2020 Elsevier B.V. All rights reserved.
L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

mineralizable C, contributing to soil metabolic activity (Brandan et al., Table 1

2017). Soil chemical and physical attributes at 0-20 cm depth under different systems
The diagnosis of soil use and management can be made using in- of use and management in Northern Minas Gerais, Brazil.
dicators such as microbiota and SOM fractions since they are sensitive Soil attributes NV (1)
SPS1 (2)
SPS2 (3)
RS (4)

to changes in environments related to agricultural production. Thus, the

use of these indicators allows the identification of sustainable man- Total sand (g kg-¹) 420 520 530 520
Silt (g kg-¹) 300 270 250 240
agement strategies for the maintenance of productivity in cultivated
Clay (g kg-¹) 280 210 220 240
soils (Frazão et al., 2010). Silt / Clay 1.07 1.28 1.13 1.00
Given this above, the aim of this study was to compare the soil C and pH(5) 5.4 5.4 5.3 5.9
nitrogen (N) stocks and quality of SOM in an Eutric Haplic Cambisol SB(6) (cmolc dm-³) 8.6 6.0 6.2 4.9
t(7) (cmolc dm-³) 8.6 6.1 6.3 4.9
after four years conversion of degraded pastures into silvopastoral
T(8) (cmolc dm-³) 12.9 9.7 9.7 8.2
systems in Northern Minas Gerais State, Brazil. We hypothesized that (i) Ca(9) (cmolc dm-³) 5.2 4.2 3.8 2.8
the introduction of integrated production systems can promote in- Mg(10) (cmolc dm-³) 2.7 1.4 2.0 1.6
creases in soil C and N stocks in the Brazilian Cerrado; and (ii) silvo- Al+3(11) (cmolc dm-³) 0 0.1 0.1 0
pastoral systems contribute to increasing soil microbial C and to redu- m(12) (cmolc dm-³) 0 1.6 1.5 0
V(13) (%) 66.6 61.8 63.9 59.7
cing the CO2 emissions into the atmosphere.
(1) NV: Native Vegetation; (2) SPS1: Integrated system with cloeziana eu-
calyptus and marandu grass; (3) SPS2: Integrated system with eucalyptus uro-
2. Material and methods grandis and Marandu grass; (4) RS: Regenerating stratum. (5) pH in water. (6)
Exchangeable base sum. (7) Effective cation exchange capacity. (8) Effective
2.1. Study site and plantation establishment cation exchange capacity at pH 7. (9) Calcium. (10) Magnesium. (11)
Potassium. (11) Exchangeable aluminum. (12) Saturation by Aluminum. (13)
The research was conducted at the Barra Farm in Francisco Sá, MG, Base Saturation. Chemical characterization performed according to metho-
Brazil (16°38′44.02″S 43°42′43.77″ W) (Fig. 1), from January 2016 to dology proposed by Embrapa (1997).
July 2017. The area is characterized by Haplic Cambisol (WRB, 2006),
with loam texture and medium soil fertility (Table 1). The region is The experimental area was a native forest until 1998 when it was
located in a transition between Cerrado and Semideciduous Seasonal converted to a pasture using Urochloa brizantha (syn. Brachiaria bri-
Forest, and its relief is flat. According to the Köppen climate classifi- zantha), commonly known as marandu grass. The area was extensively
cation, the climate is Tropical Savanna (Aw), with rainy summer and grazed for 13 years by dairy cows without soil management or re-
dry winter, and the altitude is 590 m. Annual precipitation is between placement of nutrients contents. After 2011, the pasture of marandu
1100 and 1200 mm, but the mean of annual rainfall in the evaluation grass was replaced by spontaneous vegetation, constituting a re-
period (2016–2017) was about 800 mm. The air temperature ranges generating stratum. In 2012, an area of 3.2 ha was converted to an
from 20 to 28 °C, and the mean of 25 °C was found in the evaluation agrosilvopastoral system, consisting of the integration of two species of
period. eucalyptus, sorghum, and marandu grass cultivated in the same area.

Fig. 1. Location map of the experimental area in Northern Minas Gerais, Brazil.

2
L.L.d.S. Almeida, et al.
Fig. 2. Schematic representation of the silvopastoral systems (2a) and after 4 years of implantation areas (2b) in Northern Minas Gerais, Brazil.
The spatial arrangement of the systems was: double rows of eucalyptus
(3 × 2 m), 3 m between rows and 2 m between plants, and spaces of
14 m between double rows (Fig. 2).
In December 2012, the integrated system was planted with eu-
calyptus intercropped with sorghum, which was harvested in May 2013
and used for silage. In November 2013, the sorghum was planted again
with marandu grass between double rows of eucalyptus. The second
harvest of sorghum for silage was carried out in April 2014. On the
other hand, the pasture did not have a good yield due to a long period
of drought. In November 2014, soil tillage with a disc harrow, to a
depth of 20 cm, was performed. At the same time, marandu grass,
which was planted in combination with eucalyptus, was receding. At
this point, eucalyptus trees were pruned, and after these management
operations, the area remained as a silvopastoral system with an ar-
rangement composed of eucalyptus and marandu grass.
2.2. Experimental design and treatments
The experimental design was blocs completely randomized, in the
4 × 4 factorial scheme, being four types of land use management and
four soil depths (four treatments areas and four points of soil samples),
using an area of 2500 m2 for each evaluated treatment, namely:
- Silvopastoral system using Eucalyptus cloeziana in combination with
Urochloa brizantha (marandu grass) - (SPS1);
- Silvopastoral system using Eucalyptus urograndis (E. urophylla x E.
grandis) in combination with Urochloa brizantha (marandu grass) -
(SPS2);
- Regenerating stratum (RS): area previously cultivated with pasture
of Urochloa brizantha (marandu grass), which at the time of eva-
luation presented spontaneous vegetation;
- Native vegetation (NV): reference area, secondary forest character-
ized by typical vegetation of transition areas between Cerrado and
Seasonal Semideciduous Forest.
The silvopastoral systems (SPS1 and SPS2) differed only in terms of
the eucalyptus genotypes used. The E. cloeziana specie, used in SPS1,
was chosen due to its high quality of wood, being recommended for
energy purposes (direct burning or charcoal) and civil construction. On
the other hand, the hibrid E. urograndis, used in SPS2, was chosen be-
cause it is widely used in Brazil and has greater adaptability to regions
with water stress.
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Soil & Tillage Research 205 (2021) 104785
2.3. Soil sampling
Soil sampling was carried out between 2016 and 2017. In February
2016, four mini-trenches of 40 × 40 × 50 cm were opened considering
the heterogeneity of the silvopastoral systems, with half of these soil
samples being collected between the double rows of eucalyptus and half
between the planting line of forage grasses. Into of the mini-trenches
four soil cores were taken from layers at 0–10, 10–20, 20–30, and
30–40 cm depths, and for each soil depth were collected four soil
samples to form one composite sample. These composite samples
(n = 4) were air-dried, sieved to 2 mm, and subsamples were ground
and sieved to 0.150 mm, and used to determination of total C and N
contents, and granulometric and humic fractions of SOM. Four soil
samples (n = 4) were taken for each soil depth at the same mini-tren-
ches cited before to determine soil bulk density using the volumetric
ring method described by Embrapa (1997).
To determine the microbiological attributes, soil sampling was
carried out in January (hot and humid) and July 2017 (cold and dry) at
the same mini-trenches. Samples were taken from layers at 0–5, 5–10,
and 10–20 cm depths. The samples were sealed in airtight bags, leaving
bags filled with air to avoid oxygen deficiency, and then gently packed
into coolers with ice before returning then to the Federal University of
Minas Gerais. In the lab, for each soil depth four samples were com-
bined to form one composite sample. These composite samples were
sieved to 2 mm and small plant fragments were removed to avoid po-
tential interferences in the analyses and immediately stored in a walk-in
cooler at 4 °C for further analyses.
2.4. Soil C and N stocks and C associated with soil organic matter fractions
The C and N contents were obtained using an elemental analyzer
(TruSpec, LECO Corporation, St. Joseph, MI, USA), estimating C con-
tent by infrared absorption and the total N by thermal conductivity. In
order to calculate C or N stocks in Mg ha−1, the C or N (%) content was
multiplied by the soil bulk density (Mg m-3) and the respective soil
depth layer (m).
The determination of granulometric fractions of soil organic matter
(SOM) was performed according to a methodology adapted from
Christensen (1985, 1992). Soil samples were sonicated in an ultrasonic
processor (Vibra Cell, Sonics, Inc., USA) for 25 min with an amplitude
of 53 % with 1028.57 J mL−1 of energy. After dispersion, wet sieving
was performed in 0.053 mm sieves. Particles > 0.053 mm were
L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

separated in free light fractions (FLF) and sand (Fsand) by density,

while the silt and clay (Fsilt + clay) fraction passed through the sieve
(< 0.053 mm). The three fractions were dried at 65 °C until a constant
mass was reached, and subsamples were ground and sieved to
0.150 mm for determination of C content using the elemental analyzer.
The humic fractions of SOM were determined according to a
methodology adapted from Swift (1996), using 0.5 g of air-dried soil
and 0.1 mol L−1 sodium hydroxide (NaOH) solution to dissolve the
fulvic (FA) and humic acids (HA). The humin fraction (HF) was pre-
cipitated after three cycles of centrifugation and extraction, and dried
in a laboratory oven at 45 °C. To separate the alkaline extract (AE
{FA + HA}), the pH was adjusted to 2.0 ± 0.1 with 20 % sulfuric acid
solution. The C content was determined using the methodology pro-
posed by Yeomans and Bremner (1988). After the determinations of C
content in the humic fractions, the relationship between soluble alka-
line fractions (HAF/FAF) and alkaline extract and humin fraction (AE/
HF) was calculated.

2.5. Soil microbial activity

The determination of soil microbial C (Cmic) was performed by the

fumigation-extraction method, according to Vance et al. (1987) and
adapted by Silva et al. (2007a). Additionally, microbial activity was
estimated by the determination of soil basal respiration (SBR), ac-
cording to the methodology proposed by Jenkinson and Powlson (1976)
and adapted by Silva et al. (2007b). Closed containers with 100 g of soil
and vases with 20 mL of NaOH were used to recover the evolved C
(C−CO2) emitted during the respiration of soil microorganisms. The
CO2 emissions (mg C−CO2 kg−1 soil h-1) was evaluated at each 24 h (3
evaluations), 48 h (2 evaluations), 72 h (3 evaluations), and 120 h (3
evaluations), totaling 31 days of evaluation. After the evaluation of
Cmic and SBR, the soil microbial quotient (qMIC) was calculated by the
ratio between the Cmic and soil organic C and the soil metabolic quo-
tient (qCO2) was obtained by the ratio between SBR and Cmic
(Anderson and Domsch, 1993).
Soil respiration was measured using an automated soil carbon di-
oxide (CO2) flow system (LCpro-SD, Opti-Sciences Inc., Tyngsboro, MA,
USA) coupled to a polyethylene bell (ADC Soil Hood, Analytical
Development Company Bioscientific Ltd, Hoddesdon, England) model.
The flows were estimated by the increased rate of CO2 concentration Fig. 3. Soil carbon (C) and nitrogen (N) contents (g kg−1) and C: N ratio under
inside the chamber, which was deployed on the soil surface for a short different use and management systems in the Barra Farm in Northern Minas
Gerais, Brazil. NV, Native Vegetation; SPS1, Integrated system with E. cloeziana
period of time. Measurements were taken in January (rainy season) and
and marandu grass; SPS2, Integrated system with E. urograndis and marandu
July (dry season) 2017.
grass; RS, Regenerating stratum.

2.6. Statistical analysis

The variables evaluated were submitted to the analysis of variance
(ANOVA) and the means compared by the Tukey test (p < 0.05) using
the R Statistical Software Packages, version 3.4.3 (R Core Team, 2017).
3. Results
3.1. Soil C and N stocks
Total C and N contents showed significant differences (p < 0.05)
only in the 0–10 cm layer (Fig. 3). The results revealed no significant
differences (p < 0.05) in the C:N ratio between different land uses and
management systems, which ranged from 10.36 to 14.85 for the eval-
uated soil depths.
The soil bulk density ranged from 1.18 to 1.51 Mg m−3 and did not
differ between the evaluated systems and soil depths, but the integrated
systems promoted an increase in the C and N stocks in the subsurface,
with significant reductions only evident in the 0–10 cm layer when
compared to native vegetation (Fig. 4). After four years of silvopastoral
systems (SPS1 and SPS2) introduction, both land use managements
showed an increase in C and N stocks when compared to regenerating
stratum (RS), but still lower than NV. Values ranged from 13.42 Mg
ha−1 to 39.59 Mg kg−1 and 1.29 Mg ha−1 to 3.56 Mg kg−1 for C and N
stocks, respectively.
3.2. C associated with fractions of SOM
A higher percentage of C associated with Fsilt + clay was observed,
followed by Fsand and FLF. The silvopastoral system composed of E.
cloeziana in combination with marandu grass (SPS1) was the one that
contributed the most to C protection (67.87–75.63 %) in Fsilt + clay up
to 40 cm depth (Fig. 5).
Native vegetation showed higher values of FLF in the superficial
layer, representing 22.24 % of the total organic C at this SOM fraction.
In this treatment (reference area), the C levels associated to FLF were
superior in relation to the other treatments in the superficial layer, with
reductions of 67.82 %, 65.21 %, and 72.46 % for SPS1, SPS2, and RS,
respectively. No significant differences (p < 0.05) were found between
the systems of land use in the deeper layers.
The lower C retention in Fsand was influenced by soil texture (loam
texture; Table 1) and the greater protective effect of the C by Fsilt +
clay. The lowest C content associated with Fsand was found in SPS1

4
L.L.d.S. Almeida, et al.
Fig. 4. Soil C and N stocks (Mg ha−1) under different use and management
systems in Northern Minas Gerais, Brazil. NV, Native Vegetation; SPS1,
Integrated system with E. cloeziana and marandu grass; SPS2, Integrated system
with E. urograndis and marandu grass; RS, Regenerating stratum. Vertical bars
followed by the same lowercase (treatments) and uppercase (depths) did not
differ according to Tukey test (p < 0.05).
(Fig. 5). For Fsilt + clay, no significant differences (p < 0.05) were
observed in C content between the systems, although one of the eval-
uated silvopastoral systems (SPS1) presented a 7.1 % increase in C in
relation to native vegetation.
In relation to the humic fractions of SOM, we found that most of the
C content was protected in the HF (ranging from 5.62 g kg−1 to 23.23 g
kg−1), followed by HAF and FAF (Fig. 6). The silvopastoral system SPS2
promoted the highest rates of humification of SOM, considering that 72
% of the C was protected in the HF. In addition, the predominance of HF
in subsurface layers in this system was due to lower influence of bio-
logical and environmental variables. On the other hand, the highest
solubility of SOM was observed in the silvopastoral system SPS1, which
presented 52 % of C associated to HF and greater representation in AE
(FAF + HAF).
There was no interaction (p < 0.05) between evaluated systems
and soil depths for the relation HAF/FAF, however the values were
higher than 2.58, indicating greater C content in HAF (Fig. 7). For the
EA/HF ratio, the values were smaller than 1.0; except for NV
(20–30 cm), that presented similar values for both parameters (EA and
HF). As silvopastoral system SPS2 showed 72 % of C content associated
with HF, the area had a low EA/HF ratio, ranging from 0.20 to 0.48.
3.3. Soil microbiological activity
Soil microorganism activity was evaluated by Cmic and SBR and
changed as a function of seasons (Tables 2 and 3). In January 2017,
Cmic values ranged from 144.29–424.71 mg kg−1 and in July between
318.53 and 57.17 mg kg−1, mainly increasing in subsurface layers of
both silvopastoral systems (SPS1 and SPS2) in the rainy season.
The SBR values ranged between 2.40 and 5.28 mg C−CO2 kg−1 soil
day−1 in the wet season (January 2017) and between 11.28 and
14.4 mg C−CO2 kg−1 soil day−1 in the dry season (July 2017; Tables 2
and 3). We found that, in January, regenerating stratum presented si-
milar results to native vegetation at 0–5 and 10–20 cm soil depths.
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Soil & Tillage Research 205 (2021) 104785
The Cmic and qMIC values were higher in the rainy season
(January) than in the dry period (July), with low SBR and qCO2 values
indicating greater soil microorganism stability. In the cold and dry
period, high SBR and low Cmic contents were observed, except in SPS2,
that presented a higher Cmic value in the 0–5 cm depth layer. On the
other hand, high values of qCO2 in SPS1 (16.47 mg C−CO2 kg−1 soil
h−1) in July (Table 2).
Regarding the soil CO2 efflux was affected by climatic conditions
throughout the year, ranging from 0.92 to 1.60 μmol CO2 m−2 s-1 in
January (rainy season) and from 0.19 to 0.84 μmol CO2 m−2 s-1 and
July (dry season; Fig. 8).
4. Discussion
4.1. C and N stocks in different land use and management systems
After four years of silvopastoral systems (SPS1 and SPS2) in-
troduction in an Eutric Haplic Cambisol, it was possible to observe an
increase in soil C and N levels in relation to the Regenerating Stratum
(RS; Fig. 3). These results can be attributed to the initial management of
the system, which was carried out without soil rotation (no-till), with
sorghum cultivation in the first two years and the subsequent in-
corporation of straw. In addition, the management of marandu grass
promoted good soil cover and constant renewal of the root system,
while the management of eucalyptus with pruning operations con-
tributed to the input of litter to the soil leading to an increase of C and N
contents in relation to Regenerating Stratum.
The increase in soil C and N stocks (Fig. 4) in the surface layer
(0–10 cm soil depth) in silvopastoral systems observed in this study was
higher than those found by Wendling et al. (2011) in an Oxisol after ten
years of the implementation of integrated production systems culti-
vated with eucalyptus and Brachiaria. The contribution of residues in-
puts, although lower than that observed in native vegetation, in addi-
tion to the decrease of soil disturbance, also contributed to the increase
of C and N in deeper layers (Howlett et al., 2011).
The dynamics of soil C and N can be altered over time due to the
greater sustainability conferred by the system, resulting from greater
interactions between vegetal and animal components with the soil and
influencing the soil C and N stocks (Sacramento et al., 2013). The re-
sults found in this study, after four years of silvopastoral systems (SPS1
and SPS2) implementation confirm the potential accumulation of soil C
and N, although in this case it was not enough to promote an increase in
stocks (0–40 cm) comparable to native system (NV). Agreeing with the
results found by Lim et al. (2018) evaluating different composition of
agroforestry systems, soil C stocks in the surface of mineral soil is more
responsive to changes in land-cover type. Therefore, continuous mon-
itoring is necessary to verify the accumulation of C and N in the
medium and long-term in deep layers.
4.2. Preservation of C in SOM fractions
Our findings pointed out that the C is occluded in the most stable
granulometric fractions (Fsilt + clay) of soil organic matter (Fig. 5),
confirming the importance of the silt and clay fractions for the ag-
gregation of SOM (Guardiola et al., 2017) and physical protection of
soil C (Martins et al., 2009). As we found in this study, several authors
have reported an increase in the levels of C associated with Fsilt + clay
of Oxisols in conservationist management systems (Guareschi et al.,
2013; Gazolla et al., 2015).
Regarding the FLF, the rainy season increased soil humidity and
metabolic activity and, consequently, the availability of C that could be
readily mineralized or oxidized in the native vegetation. There is con-
stant deposition of residues and absence of anthropic interventions in
this system. On the other hand, the soil under silvopastoral systems
were disturbed by harrowing for planting Marandu grass in 2014,
which may have contributed to the reductions of C due the
L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

Fig. 5. Distribution of the C content (%) in the in granulometric fractions of SOM at 0-10 (A), 10-20 (B), 20-30 (C) and 30-40 cm (D) soil depths under different
systems of use and management systems in Northern Minas Gerais, Brazil. NV, Native Vegetation; SPS1, Integrated system with E. cloeziana and marandu grass; SPS2,
Integrated system with E. urograndis and marandu grass; RS, Regenerating stratum. FLF, free light fraction; Fsand, Fraction of sand; Fsilt + clay, fraction of silt and
clay. Vertical bars followed by the same lowercase (treatments) and uppercase (depths) did not differ according to Tukey test (p < 0.05).

mineralization processes (Brandan et al., 2017).
The lower C content associated to Fsand in SPS1 (Fig. 5) can be
attributed to greater consumption of organic materials by soil micro-
biota. On the other hand, the increase in C content associated to
Fsilt + clay in the silvopastoral system (SPS1) is an indication that, in
the long term, integrated production systems can recover soil C content
in stable fractions of SOM (Guareschi et al., 2013; Gazolla et al., 2015).
Regarding the higher C content associated to humin fraction (HF) in
the different evaluated systems (Fig. 6) can be due to the low mobility
of this fraction in the soil and the structural complexity of its molecules.
In addition, conservationist systems promote less soil disturbance by
agricultural practices and tend to promote adequate conditions for
complex reactions of condensation and polymerization, allowing the
formation of more stable humic substances in soil (Ebeling et al., 2011).
As we found for silvopastoral system (SPS2), another study performed
by Gazolla et al (2015) also verified increases in C associated to humin
fraction in responses to soil management in crop-livestock integrated
systems after 19 years of implantation.
The C ratios between humic fractions (Fig. 7) confirmed the highest
C content in the stable fractions of soil organic matter. There is a
strongly influence of soil cover and granulometric composition for the
formation of more stable humic material (Valladares et al., 2008). The
lower AE/HF ratio value (0.20) was found in silvopastoral system
(SPS2), resulting in less degradation due the higher recalcitrance of
humin fraction in soil (Fontana et al., 2011). This result can be attrib-
uted to the greater contribution of residues of Eucalyptus urograndis in
SPS2 through the quality of the litter (Matos et al., 2017). Other studies
showed similar results, emphasizing the importance of organic sub-
strate for the recalcitrance of soil organic matter over time (Martins
et al., 2009; Fontana et al., 2017).
4.3. Soil microbial activity and CO2 efflux
Our results confirmed that humidity and temperature during the
rainy season (January) influenced the degradation of organic materials
by the soil microbiota, interfering in nutrient cycling and C im-
mobilization in the microbial tissue (Table 2). According to Oliveira
et al. (2016), high soil moisture and temperature due to climatic sea-
sonality can stimulate greater degradation of the organic material by
the soil microbiota.
The more intensive litter input in a silvopastoral system (SPS2) was
due the pruning operation and great input of leaves and fine branches
to the soil during the dry season, and may have influenced the activa-
tion of soil microbiota, thus allowing greater accumulation of organic

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L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

Fig. 6. Distribution of the C content (%) in the in granulometric fractions of SOM at 0-10 (A), 10-20 (B), 20-30 (C) and 30-40 cm (D) soil depths under different
systems of use and management systems in Northern Minas Gerais, Brazil. NV, Native Vegetation; SPS1, Integrated system with E. cloeziana and marandu grass; SPS2,
Integrated system with E. urograndis and marandu grass; RS, Regenerating stratum. FAF, fulvic acid fraction; HAF, humic acid fraction; FH, humin fraction. Vertical
bars followed by the same lowercase (treatments) and uppercase (depths) did not differ according to Tukey test (p < 0.05).

residues in the 0−5 cm layer and contributing to an increase in Cmic
(Table 3). Other studies with integrated production systems performed
in the Cerrado region pointed out the potential of E. urograndis in
producing additional organic matter to the soil and contributing to
ecological balance in cultivated ecosystems, with greater intensity in
the dry season (Stieven et al., 2014; Matos et al., 2017).
Both silvopastoral systems presented an increase of Cmic in deeper
layers in the wet season (Table 2). This result can be explained by the
soil management (e.g. harrowing) in these areas, with the incorporation
of residues and the implementation of Marandu grass in 2014. As ob-
served in this study Oliveira et al. (2016) also verified an increase of
Cmic in the soil subsurface in wet season after two years of im-
plementation of a crop-livestock system in the Brazilian Cerrado.
In general, soil microbial biomass stability was observed in the wet
season (January), evidenced by low qCO2 values in relation to July
(Tables 2 and 3). Thus, less C was lost by respiration (SBR) and there
was a greater accumulation of C in microbial tissue by immobilization
processes (Oliveira et al., 2016). The lower values observed in January
suggest efficiency in the use of organic substrate as a source of energy
for the maintenance of microbial metabolism. Furthermore, stability of
the system was observed under these conditions since high rates of
qCO2 indicate system inefficiency due to the greater loss of C by mi-
neralization processes, thus impairing soil microbial diversity (Tótola
and Chaer, 2002; Yan et al., 2009). The higher values of qCO2 in the
silvopastoral system (SPS1) in July (Table 2) reflected higher environ-
mental disturbance due to low immobilization of organic C by the soil
microbiota (qMiC) and high SBR.
The highest variations in SBR during the two periods were observed
in the 0–5 and 10–20 cm, probably because they cover regions of in-
fluence near the surface (contribution of residues) and rhizosphere
(release of organic compounds), respectively. As observed by Frazão
et al. (2010) the higher soil basal respiration in periods of water deficit
relate to a response to stress conditions and low efficiency in the con-
version of organic C to Cmic due to higher expenditure of C (energy) to
maintain microorganisms in the soil (Anderson and Domsch, 1993;
Islam and Weil, 2000). However, low respiratory activity may be

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L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

Fig. 7. C ratio between humic acid and fulvic acid fraction (FAF/HAF) and between alkalin extract and humin fraction (AE/HF) at 0-10 (A), 10-20 (B), 20-30 (C) and
30-40 cm (D) soil depths under different systems of use and management systems in Northern Minas Gerais, Brazil. Vertical bars followed by the same lowercase
(treatments) and uppercase (depths) did not differ according to Tukey test (p < 0.05). *No significant interaction was observed for the FAF/HAF ratio. NV, Native
Vegetation; SPS1, Integrated system with E. cloeziana and marandu grass; SPS2, Integrated system with E. urograndis and marandu grass; RS, Regenerating stratum.

indicative of low specific activity of soil microbiota (Almeida et al.,
2016).
The qMIC values indicated that different sampling conditions (wet
and dry seasons) interfere in the soil microbial population balance,
especially in integrated systems and deeper layers, in dry and cold
periods (Tables 2 and 3). Therefore, values lower than 1% in July in-
dicated the existence of limiting factors to the activity of microorgan-
isms in the soil, with values ranging from 2% to 5% on SOM, already
used as reference in a previous study (Jenkinson and Ladd, 1981) were
considered adequate.
The higher CO2 efflux in the wet season was influenced by ideal
conditions of temperature and humidity in January (Fig. 8), allowing
intense degradation of organic residues and CO2 release. Also, roots and
organism activities in the different evaluated systems are factors that
contribute to greater soil respiration (Arevalo et al., 2010). We ob-
served that SPS1 presented high values of Cmic in the superficial layer
(0–5 cm) during the wet season, a fact that can justify the high efflux of
CO2 during this period.
As observed for Cmic values, CO2 efflux was higher in areas with
higher inputs of residues over time (Native Vegetation and
Silvopastoral Systems). The results obtained for Regenerating Stratum
can be associated to the lower plant diversity, which contributed to
lower activity of soil organisms. In January, the largest efflux of CO2
can be also explained by intensive biological activity in soil. However,
low soil moisture in July decreased microbial activity and CO2 efflux in
all evaluated systems. According to Pinto-Junior et al. (2009) low soil
moisture limits the degradation of SOM by soil microorganisms,
reducing C−CO2 losses from soil to atmosphere. However, in this
study, the evaluated silvopastoral systems showed lower CO2 efflux in
both rainy and dry season was lower than those observed by Pinto-
Junior et al (2009). We infer that this result is due to the low rate of soil
disturbance in the integrated production systems after four years of
implantation.
5. Conclusions
Integrated production systems promoted an increase in soil C and N
stocks after four years of implementation. Nevertheless, long-term
monitoring is necessary to verify if storage can be similar to levels
found in native vegetation over time.
We observed that, in all evaluated systems, soil C content is pro-
tected in the most stable fractions of the SOM (HFUM and Fsilt + lay)
and subsurface.
Integrated production systems contributed to increasing soil Cmic
with low rates of CO2 emissions due to substrate diversity for microbial
population growth and soil activity, reflecting an increase in nutrient
cycling efficiency and maintenance of N stocks.
Declaration of Competing Interest
I declare that the authors “Luana Larrisa de Souza Almeida, Taynan
Aquilles Marinho Lessa, Luiz Arnaldo Fernandes, Álvaro Luiz de
Carvalho Veloso, Angela Maria Quintão Lana, Igor Alexandre de Souza,
Rodinei Facco Pegoraro, Evander Alves Ferreira, Leidivan Almeida

8
L.L.d.S. Almeida, et al. Soil & Tillage Research 205 (2021) 104785

Table 2
Soil microbiological attributes in January 2017 under different systems of use
and management in Northern Minas Gerais, Brazil.
Systems 0−5 cm 5−10 cm 10−20 cm

Cmic (mgk kg-1)(5)

NV(1) 366.30 aAB 373.72 aA 227.20 Bb
SPS1(2) 341.30 aA 356.4 abA 424.71 Aa
SPS2(3) 144.29 bA 241.80 abA 259.13 abA
(4)
RS 282.64 abA 186.86 bA 186.36 Ba
SBR (mg C-CO2 kg-1 soil day-1)(6)
NV 3.60 bA 2.88 aB 2.40 Bb
SPS1 3.60 bA 3.12 aA 3.12 abA
SPS2 3.84 bA 2.88 aB 3.84 aA
RS 5.28 aA 3.12 aB 2.64 bB
qCO2(mg C-CO2 kg-1 soil h-1)(7)
NV 0.42 bA 0.34 aA 0.46 aA
SPS1 0.47 bA 0.43 aA 0.33 aA
SPS2 2.00 aA 0.54 aB 0.62 bA
RS 0.83 bA 0.84 aA 0.94 aA
qMIC(%)(8)
NV 1.39**(9) 1.96** 1.30**
SPS1 2.02 2.33 2.87
SPS2 0.94 1.88 2.11 Fig. 8. Soil CO2 efflux (μmol CO2 m−2 s-1) in January and July 2017 (wet and
RS 2.63 3.46 3.76
dry seasons) under different systems of use and management in Northern Minas
Gerais, Brazil. The vertical bars followed by the same lowercase letter (treat-
(1) Native vegetation, (2) Silvopastoral system with E. cloeziana + Marandu
ments for the same period) and uppercase (treatments between the evaluated
grass, (3) Silvopastoral system with E. urograndis + Marandu grass, (4)
epochs) did not differ according to Tukey test (p < 0.05). NV, Native
Regenerating Stratum, (5) Microbial Carbon, (6) Soil Basal Respiration; (7)
Vegetation; SPS1, Integrated system with E. cloeziana and marandu grass; SPS2,
Metabolic quotient; (8) Microbial quotient. (9) No effect was observed for in-
Integrated system with E. urograndis and marandu grass; RS, Regenerating
teraction (systems x depths). Means followed by the same lowercase letter in
stratum.
the column indicate similarity between treatments and, the uppercase, equality
between depths by the Tukey test (p < 0.05).
Acknowledgements
Table 3
Soil microbiological attributes in July 2017 under different systems of use and This work was supported by the National Program of Academic
management in Northern Minas Gerais, Brazil. Cooperation from “Coordenação de Aperfeiçoamento de Pessoal de
Systems 0−5 cm 5−10 cm 10−20 cm Nível Superior” – CAPES/Brazil (Grant number 88881.068513/2014-
01); “Fundação de Amparo à Pesquisa do Estado de Minas Gerais” –
mic (mgk kg-1)(5) Fapemig (Grants number APQ-00953-14, PPM-00133-15); and
NV(1) 318.53 aA 147.01 aB 81.67 abB
“Conselho Nacional de Desenvolvimento Científico e Tecnológico” –
SPS1(2) 285.86 abA 138.84 aB 57.17 Bb
SPS2 (3)
212.35 abA 236.85 aA 204.18 aA CNPq (Grant number 430097/2016-6). We thank to Pró-Reitoria de
RS(4)
187.85 ba 114.34 aA 106.17 abA Pesquisa of Universidade Federal de Minas Gerais (UFMG) for providing
SBR (mg C-CO2 kg-1 soil day-1)(6) language help. We also thank to Barra Farm for all the logistic support
NV 13.92 aA 13.2 aA 11.52 bB given during this study.
SPS1 11.52 bB 12.24 aAB 13.68 aA
SPS2 14.4 aA 13.20 aA 11.28 bB
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