Geoderma Regional 5 (2015) 1524

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Geoderma Regional
journal homepage: www.elsevier.com/locate/geodrs

SOC dynamics and soil quality index of agroforestry systems in the

Atlantic rainforest of Brazil
A. Thomazini a,, E.S. Mendona a, I.M. Cardoso b, M.L. Garbin a
a
b

Department of Plant Production, Federal University of Esprito Santo, 29500-000 Alegre, Esprito Santo, Brazil
Soil Science Department, Federal University of Viosa, Avenida P. H. Rolfs, s/n, 36570-000 Viosa, Minas Gerais, Brazil

a r t i c l e

i n f o

Article history:
Received 17 December 2014
Received in revised form 20 February 2015
Accepted 23 February 2015
Available online 4 March 2015
Keywords:
Soil health
Agroforestry
Land use
Soil carbon
PCA
Ferralsol
Oxisol

a b s t r a c t
Land cover change and implementation of different management practices can greatly affect the global carbon
(C) budget and soil quality. The objective of this study was to quantify the effect of different management practices under representative agroforestry and full sun coffee systems on (i) soil organic matter and CO2C emissions
in dry and rainy seasons and (ii) to determine which management system of coffee is the most effective for improving soil quality in the Atlantic Rainforest Biome. A plot of 300 m2, divided into three subplots of 100 m2 each,
was established in three sampling sites: an agroforestry coffee system (ACS), a full sun coffee system (FS) and a
native rainforest (NR) (chosen as reference site of soil conservation). Soil sampling was carried out at ve different depths (05, 520, 2040, 4060 and 60100 cm) for soil chemical and organic matter characterization in
each subplot. CO2C emissions, soil temperature, moisture and microbial biomass C were measured four times
in one year. The soil quality index (SQI) was evaluated with a principal components analysis (PCA) to compare
soil quality classes among the selected sites. ACS tended to has the highest soil C content (19.8 g kg1) in the
05 cm soil layer. FS tended to has less C and nitrogen (N) stock values and elevated metabolic quotient. The
CO2C emissions at the ACS site decreased 1.93 Mg CO2C ha1 year1 when compared to the FS system. An
overall trend of lower labile C was recorded up to 40 cm depth in the FS system (36% less). The ACS provided continuous input of labile organic matter fractions to the soil by litterfall contributing to a continued incorporation of
soil C. The results indicated that CO2C emission, soil temperature, metabolic quotient, C/N ratio, labile and soluble C were the most important soil quality indicators, reecting the general biological properties of the soil.
Based on the SQI values, ACS is the most suitable management of coffee, since it preserves soil quality. Management strategies that guarantee a continued and diversied input of organic matter enable the following:
(i) increased C soil storages, (ii) the stabilization of the microbial biomass C, (iii) a reduction in C loss through
CO2C emissions and (iv) the best indices of soil quality. These are crucial targets in order to restore soil quality
in the Atlantic Rainforest Biome.
2015 Published by Elsevier B.V.

1. Introduction
The coffee plant crop is one of the main agricultural activities in
Brazil, generating income and employments to the Brazilian agriculture.
The crop is mainly produced by family smallholders, who keep the
farmer in the countryside and contribute to regional socio-economic development (Moo et al., 2009; Souza et al., 2010). Conversion from natural to agricultural systems, as coffee crop or other land use, has largely
contributed to the degradation of Brazilian Atlantic rainforest. Most of
the smaller numerous remaining forest fragments are poorer in species
richness and have lower soil quality than larger and well-preserved
fragments, characterizing degraded ecosystems (Moo et al., 2009;
Gama-Rodrigues et al., 2010; Souza et al., 2012; Duarte et al., 2013).
Corresponding author.
E-mail addresses: andre.thz@gmail.com (A. Thomazini), esmjplia@gmail.com
(E.S. Mendona), irene@ufv.br (I.M. Cardoso), mlgarbin@gmail.com (M.L. Garbin).

http://dx.doi.org/10.1016/j.geodrs.2015.02.003
2352-0094/ 2015 Published by Elsevier B.V.

Full sun coffee production is generally associated with intensive

crop cultivation and unsustainable agricultural practices, leading to
breakdown of soil aggregates, exposing encapsulated C to decomposition and increasing CO2C emission (Anderson and Domsch, 2010;
Gama-Rodrigues et al., 2010). As a consequence, more nutrients are
being released due to organic matter mineralization in full sun coffee
systems (Gama-Rodrigues et al., 2010). Conventional till can decrease
the soil organic C pool and structural stability, generating severe environmental changes (Lal, 2004). These systems can promote losses of
chemical, physical and biological soil quality in both short and longterms. This is directly related to low crop productivity and a decrease
in the smallholder's livelihoods.
Soil organic matter is highly sensitive to change through management and is widely used as an indicator of soil quality. Soil quality assessment is essential to quantify the effects of human actions and
improper management on the agroecosystem, mostly those related to
the sustainability of the agriculture (Armenise et al, 2013; Lu et al.,

16

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

2014). Surface soils (030 cm depth) store almost half of soil organic C
and up to three times of the above-ground C stored in a vegetation.
Moreover, they are vulnerable to losses as CO2C emissions due to climatic changes and land management practices (Powlson et al., 2011).
The total quantity of organic C in soils is approximately 1500 Pg (Lal,
2004), which is approximately two times the C content present in the
atmosphere (Lal, 2004). Changes in soil organic C will produce obvious
undesirable consequences on the current patterns of climate change.
Thus, the soil C pools may act as a source of atmospheric C (Davidson
and Janssens, 2006). However, with the adoption of sustainable land
management practices, agricultural ecosystems can potentially be a
sink of atmospheric C and reduce greenhouse gas emissions (Lal,
2004; Davidson and Janssens, 2006; La Scala et al., 2009; Liebig et al.,
2013; Song et al., 2013). In this context, there has been increasing
concern in recent years about the consequences of tree planting in coffee plantations and the resulting effects on C sequestration and soil
quality.
Even though full sun is the dominant management system in the
Brazilian coffee agriculture, there has been an increase in the agroforest
and agroecological practices in the country (Souza et al., 2010). A more
diversied agricultural matrix using agroforestry, where native trees are
intercropped with coffee, has been regarded as one of the best options
for conservation, regeneration and reforestation of the Atlantic
Rainforest Biome (Moo et al., 2009; Souza et al., 2010, 2012; Duarte
et al., 2013). The organic material (above-and belowground litter) produced by trees in agroforestry systems protects the soil against erosion,
serves as food for soil organisms, improves soil structure, and contributes to nutrient cycling, thus increasing nutrient availability to plants
(Nair et al., 2009; Matos et al., 2011; Souza et al., 2012). Soil surfaces
covered by plant organisms and without soil disturbance result in a
gradual decomposition of organic material, which is maintained in the
soil for a long time (Pezarico et al., 2013).
The main chemical and biochemical processes related to soil CO2C
emissions are directly or indirectly related to soil temperature and
moisture, which might vary spatially and temporally in several ecosystems (La Scala et al., 2009; Cruvinel et al., 2011; Stockmann et al., 2013).
Therefore, soil CCO2 emissions are regulated by climatic conditions, especially soil temperature and soil moisture (Cruvinel et al., 2011).
Changes in soil management may affect numerous factors that are directly or indirectly related to temperature and moisture, modifying
the dynamics of soil CO2C emission (La Scala et al., 2009). These assessments are variable among tropical systems, once they are highly heterogeneous. These trends lead to changes on moisture, temperature,
nutrient and C cycling, directly affecting CO2C emissions. Analyzing
the changes on moisture and soil temperature and C storing will provide
insights that are necessary for making justiable recommendations
about the implementation of these systems and to assess soil quality
in the tropical zones.
Globally, about 10 million ha is occupied with coffee production systems (FAO, 2011). Therefore, their design and management may have
profound effects over land-based C ux and storage. The increase of
soil organic C pools is a key in order to mitigate and adapt strategies related to climatic changes. Two aspects are imperative in identifying effective strategies for land-based climate change mitigation under
possible future climate change scenarios: rstly, we need to identify
how different agricultural management practices or changes in landuse create soil organic C sinks (accumulating additional C); secondly,
how they act as C sources (emitting C) or maintain stocks at current
levels. The objective of this study was to quantify the effect of different
management practices under representative agroforestry coffee system
(ACS) and full sun coffee system (FS) on (i) soil organic matter and CO2
C emissions in dry and rainy seasons and (ii) to determine which coffee
management system is the most effective for improving soil quality in
the Atlantic Rainforest Biome. It is hypothesized that (i) the transition
from FS to ACS reduces CO2C emissions to the atmosphere; (ii) ACS
increases carbon sink potential, leading to improved soil quality and

(iii) agroforestry practice is essential to draw meaningful conclusions

for climate change mitigation strategies at regional and global scales.
2. Materials and methods
2.1. Experimental site and design
The study was carried out in two family smallholders located at Feliz
Lembrana community (204752.51S 413037.72W), municipality
of Alegre, Capara region, Esprito Santo, within the Atlantic Rainforest
Biome domain. The climate of the region is Awa, characterized by dry
winter and rainy summer (see Fig. 1) (Kppen, 1923). The altitude
varies from 100 to 1.326 m above the sea. The parent rock in the study
area has granitic origin. The soil in the experimental area is a clayey
Oxisol (Red-Yellow Latosol, Brazilian Classication System, Embrapa,
2006) or as Typic Haplustox (Soil Survey Staff of USDA, 1999). The soil
is very well structured, and freely drained (A-horizon = 530 cm and
B-horizon = 50250 cm, on average) (Embrapa, 2006). Native
rainforest (NR) is a typical Atlantic Rainforest subjected to selective logging in the last 20 years. NR is mainly composed of Schinus
terebinthifolius Raddi., Cupania vernalis Cambess., Cedrela ssilis
Vell., Handroanthus heptaphyllus Mart., Handroanthus pulcherrimus
Sandwith., Matayba guyanensis Aubl., Eugenia involucrate DC., Dalbergia
nigra Vell., Anadenanthera macrocarpa Benth., and Joannesia princeps
Vell. NR was chosen as a reference site of soil conservation.
ACS was established 28 years ago in 2.4 ha on a formerly pasture
area. C. ssilis, C. vernalis, Inga sessilis and Eucalyptus sp. were allocated
in the site without specic spacing. After the two rst years, the site
was primarily managed through periodic thinning of major branches
to reduce tree density. At the same time, the farmer planted the coffee
culture (Coffea canephora) with a 2.5 2 m spacing between row and
plants, respectively. Fruit and forest trees were planted over the years,
without specic spacing, nor density control. Over the years, management of spontaneous plants was conducted by weeding. In the last
four years, the farmer has been doing it with mechanical mowing. By
the year 2010 and 2012, liming was applied (when necessary), and
manual fertilization was made, formulated with 25-5-20 (nitrogen
phosphoruspotassium) once a year, at the beginning of the rainy season. ACS has a constant above-ground vegetation cover, visually similar
to NR with high diversity of cultivated plants (mainly papaya, orange,
palm tree, cocoa, coconut, banana, tangerine). The annual production
is currently around 2030 bags of 60 kg/ha of coffee. The diversity of
plants provides sales of products in food programs and local fairs,
which provide nancial sustainability for the family farmer.
The implementation of FS took place 16 years ago in the erstwhile
pasture lands. For ten years, weeding was the main form of management of unwanted plants, with complete removal of soil cover. After

Fig. 1. Average monthly climatic data of the municipality of Alegre-ES during experiment
periods from January 2012 to January 2013.
Data from Incaper (Esprito Santo Institute for Research, Technical Assistance and Rural
Extension).

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

this, the farmer began to use chemical and mechanical mowing controls
of unwanted plants. In the last three years, only mechanical mowing has
been used. Coffee culture is spaced 2.5 2 m (between row and plants,
respectively). Fertilizations are made four times a year with the formulation 25-05-20 (NP2O5 and K2O), based on soil analysis, and liming
when it is necessary. The annual production is currently around 4060
bags of 60 kg/ha.
2.2. Soil sampling
Soil was sampled in March 2012. The soil sampling design was systematic using a sampling area divided into three experimental plots of
100 m2 each. All plots were located at elevations between 550 and
750 m. In each plot, disturbed and undisturbed soil samples were
taken at ve different depths (05, 520, 2040, 4060 and 60
100 cm). Five soil sub-samples were obtained per plot, and were then
composed into one sample. The sample areas are located in a western
exposure site and at the same watershed (downstream) for all soil management systems. Each soil sample was divided into two portions. One
part was air-dried on the same day of sampling and the other was stored
at 4 C until analysis. Soil samples were sieved through a 2-mm sieve to
remove larger pieces of root material and the stone fraction. Fresh soil
samples were used to determine moisture, microbial biomass C and soluble C. All soil samples were analyzed in the soil laboratory at the Federal University of Espirito Santo, Agriculture Science Center.
2.3. Soil chemical and physical characterization
In each site, samples were taken at A and B horizons for chemical and
physical characterization (Table 1). The pH was determined on a 1:5
soil:deionized water ratio; the potential acidity (H + Al) was extracted
with Ca(OAc)2 0.5 mol L1 buffered to pH 7.0, and quantied by titration with NaOH 0.0606 mol L1. Exchangeable Ca2+, Mg2+ and Al3+
were extracted with 1 mol L 1 KCl and P, Na and K were extracted
with Melich-1 (Embrapa, 1997). The element levels in the extracts
were determined by atomic absorption (Ca2+, Mg2+ and Al3+), ame
emission (Na+ and K+) and photocolorimetry (P). The effective cation
exchange capacity (CECE) was calculated by sum of cations (Ca2 +,
Mg2+, Na+ and K+) and total cation exchange capacity (CTCT) estimated by the sum of the CECE and potential acidity. The granulometric analysis was performed by the pipette method while bulk density (BD) was
performed by the volumetric ring method (Embrapa, 1997).
2.4. Soil organic matter
The samples collected at the ve different layers were analyzed to
total organic C (Toc), total nitrogen (Ton), labile C (Labc) and recalcitrant C (Rcalc). Total soil organic C was quantied by wet oxidation
with K2Cr2O7 0.167 mol L1 in the presence of sulfuric acid with external heating. Total N was quantied by sulfuric acid digestion followed
by Kjeldahl distillation. The fractions of soil organic C were estimated

17

through a modied Walkely and Black method as described by Chan

(Chan et al., 2001) using 2.5, 5 and 10 mL of concentrated H2SO4
resulting in three acidaqueous solution ratios of 0.25:1, 0.5:1 and 1:1
(which corresponded, respectively to 3, 6 and 9 mol L1 H2SO4). The
amount of soil organic C determined using 2.5, 5 and 10 mL of concentrated H2SO4 when compared with total C, allowed separation of total C
into the following four fractions of decreasing oxidizability: Fraction I
(very labile) organic C oxidizable under 3 mol L1 H2SO4; Fraction II (labile) the difference in soil organic C extracted between 6 and 3 mol L1
H2SO4; Fraction III (less labile) the difference in soil organic C extracted
between 9 and 6 mol L1 H2SO4; and Fraction IV (non-labile) residual
organic C after reaction with 9 mol L1 H2SO4 when compared with
total C. The sum of Fractions I and II corresponds to the labile C and
the sum of Fractions III and IV to the recalcitrant C (Chan et al., 2001).
The C and N stocks were estimated based on the equivalent soil mass
method (Ellert and Bettany, 1995), taking the soil mass of the NR as
control.
2.5. Respirometry and soil temperature
Measurements of CO2C emissions (CO2C) were made on March,
July, October 2012 and January 2013. In each subplot, six replicates in
each soil management system were sampled. CO2C emissions were
measured using a portable LI-8100 analyzer (LiCor, EUA) coupled to a
dynamic chamber (LI-8100-102), known as survey chamber with
10 cm diameter and placed on PVC soil collars inserted in the soil
(5 cm depth). Measurements at each soil management system lasted
for over 1.5 min and the measurements were made of CO2C concentrations inside the chamber at 3-s intervals (Thomazini et al., 2015). Soil
temperatures (5.0 cm depth) were determined during the gas
ux measurements. The relation between CO2C (FCO2C) and
soil temperature (Tsoil) was obtained by Eq. (1): FCO2 =
F0 exp(B Tsoil) (1), with the natural log (Ln) of the CO2C emission
we have Ln(FCO2C) = Ln(F0 exp(b Tsoil)), the result is Ln(FCO2
C) = Ln(F0) + b Tsoil. A linear relation between Ln(FCO2C) and the
Tsoil is expected when soil temperature is a limiting factor. Based on the
B coefcients it is possible to derive the Q10 factor, which represents the
percentage of increase in emission for a 10 C increase in soil temperature. This is equated as Q10 = e10xb (Carvalho et al., 2012).
2.6. Moisture and microbial biomass C
Disturbed fresh soil samples were collected to determine moisture,
microbial biomass C (Biom), soluble C (Solc), metabolic (Qmet) and microbial quotient (Qmic). They were sampled at the same depth (5 cm)
and month when CO2C emissions were measured. Soil moisture was
determined using the thermogravimetric method (105110 C for
24 h) (Embrapa, 1997). Microbial biomass C was determined by the irradiationextraction method, according to the methodology developed
by Ferreira et al. (1999). The C content was extracted with 0.5 M K2SO4
(calibrated pH 6.56.8) in non-irradiated samples and they were used

Table 1
Chemical and physical characterization of the A and B horizons of soils under different management systems in southern Espirito Santo, Brazil.
Systems

pH

H2O

mg dm3

Na

Ca

Mg

Al

H + Al

SB

CECE

A-horizon
NR
ACS
FS

4.34
5.24
5.86

9.44
10.86
6.48

69.33
111.33
101.00

2.33
1.67
2.00

0.40
1.21
0.87

0.35
0.65
0.57

0.90
0.02
0.00

9.05
2.89
2.37

0.95
2.15
1.70

1.85
2.17
1.70

10.00
5.04
4.06

9.86
42.97
46.37

48.55
0.77
0.00

B-horizon
NR
ACS
FS

4.44
4.79
4.97

2.96
2.80
1.64

21.33
42.33
42.67

3.00
2.33
1.67

0.04
0.28
0.43

0.12
0.20
0.27

1.00
0.25
0.23

5.12
2.83
3.00

0.23
0.60
0.82

1.23
0.85
1.05

5.34
3.44
3.82

4.38
18.23
21.48

81.41
29.78
23.44

CECT

cmolc dm3

Sand

Silt

Clay

638.18
638.96
623.53

55.19
73.43
48.23

306.62
287.61
328.24

525.38
433.96
568.64

68.11
98.44
64.29

406.51
467.60
367.07

g kg1

NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system; pH: active acidity; P: phosphorus; K: potassium; Na: sodium; Ca: calcium; Mg: magnesium; Al: aluminum; H + Al: potential acidity; SB: sum of bases; t: effective cation exchange capacity; T: total cation exchange capacity; S: saturation of bases; m: aluminum saturation.

18

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

to estimate soluble C. Metabolic quotient was determined by the ratio

between the soil CO2C emission rate and microbial biomass C unit,
and microbial quotient was calculated by the ratio between microbial
biomass C and total soil organic C.
2.7. Soil quality index
The soil quality index (SQI) was used to assess the soil quality under
different management systems of coffee and a NR. The indexing technique assessed here follows that proposed by Karlen and Stott (1994)
and recently used by Fernandes et al. (2011), Armenise et al. (2013)
and Lu et al. (2014). Indicators estimated in this study include 14 chemical and biological soil attributes: Total organic C, Total N, C/N ratio, Labile and recalcitrant C, C and N stock and annual mean of CO2C
emission, soil temperature, moisture, microbial biomass C, soluble C,
metabolic and microbial quotient. According to Armenise et al. (2013)
and Lu et al. (2014), the method involved three principal steps:
(i) selection of appropriate indicators through principal component
analysis (PCA), which corresponds a minimum data set (MDS) that
are the most signicant variables that best represent the soil functions,
(ii) transformation and weighting of indicators and (iii) combining the
indicator scores into a soil quality index (additive model).
For a given principal component (PC), only the indicators with high
factor loadings were retained for indexing. Kaiser criterion (Kaiser,
1960) and the Scree test (Cattell, 1966) were used to reduce the number
of indicators and PCs. The eigenvalue criterion suggests retaining any
component with an eigenvalue greater than 1.00. Each observed
standardized indicator contributes one unit of variance to the total,
therefore, a PC with an eigenvalue lower than 1.00 is accounting for
less variance than is generated by a single standardized indicator
(Armenise et al., 2013). High eigenvectors were dened as absolute
values within 10% of the highest eigenvector. If more than one indicator
was retained under a single PC, a multivariate correlation analysis was
used to determine if the indicators could be considered redundant and
eliminated from the SQI. Among well-correlated variables, the
indicator(s) with the highest eigenvector was chosen for the SQI. If
the higher indicators were not correlated, then each was considered important and was retained in the SQI (Lu et al., 2014).
The MDS were transformed into individual values (scores) ranging
from 0 to 1. Score equals to 1 represents the optimum level for the indicator (Armenise et al., 2013). Scoring curves were generated from the
equation proposed by Wymore (1993). Three types of standardized
scoring functions are typically used for soil quality assessment:
(i) More is better; (ii) Less is better, and (iii) Optimum. More is better
functions were used for labile and soluble C, due to their positive inuence on soil quality (if increasing the level of the indicator, the quality of
the soil increases). The optimum function was used to score soil temperature. The optimum curve scores those indicators that have an increasingly positive association with soil quality up to an optimal level beyond
which soil quality decreases (Lu et al., 2014). Less is better functions
were used for soil CO2C emission, metabolic quotient and C/N ratio,
that indicate poor soil quality at high levels (increment negatively affects soil quality) (Wymore, 1993). The proper curve type for each indicator, baseline, threshold values, slope and the corresponding critical
limits were assigned as suggested by Lu et al. (2014).
The scores were combined into an overall SQI, according to the following equation (Eq. (2))
SQI

Xn
i1

WiSi;

where, W is the PCA weighting factor of the indicator selected by PCA

and S is the corresponding score generated. The results may range
from 0 to 1. This additive model proposed by Karlen and Stott (1994),
suggest that when the soil SQI is 1, the soil presents the highest quality
for the evaluated function. In contrast, when SQI is 0, it indicates a low
soil quality or a much degraded soil.

2.8. Data analysis

Statistical analyses, including descriptive statistics, Pearson correlations and principal component analysis, were performed using SAS
(SAS version 9, SAS Institute, Cary, NC, USA). Results were interpreted
in terms of general trends (mean and standard error) due to soil management, since sites are located in the same soil type and altitude
range. Principal component analysis was used to explore general trends
of soil variables and to perform soil quality index (SQI). The soil quality
indicators retained with the PCA were subjected to correlation analysis.
The soil quality approach was used as an analytical method to assess differences of management systems with lack of adequate replication.
3. Results
3.1. Soil organic matter
Mean values of total organic C, total N, C/N ratio, labile C, recalcitrant
C and bulk density in the different soil management systems are given
in Fig. 2. The highest changes in total organic C, total N, C/N ratio, labile
and recalcitrant C occurred in the 040 cm depth. In general, soil organic
matter decreased as depth increased. At 020 cm layer, FS tended
to has less total organic C, recalcitrant C and bulk density when compared to the ACS. Total organic C observed to be higher in NR and ACS
at 05 cm layer, showing similar results up to 40 cm depth. A similar
trend was observed for labile and recalcitrant C. Total N is leaning to
be higher under the NR. Total N tended to be similar in the ACS and
NR up to 20 cm depth. Minor variations of total organic C ranged from
6.31 to 7.65 g kg1 and occurred in the FS. Bulk density tended to decrease in soil depth, and NR tended to present the lowest values. Bulk
density was observed to be higher in the FS system (1.53 g cm 3 at
520 cm layer), and lower in the NR system. Bulk density tended to be
lower in the ACS system (1.30 g cm3 at 520 cm layer) when compared to FS. Carbon and nitrogen stocks' (C and N stocks) data at different soil management systems are shown in Table 2. C and N stocks were
observed to be higher in NR (125.21 and 12.82 Mg ha1). ACS tended to
store more C and N than FS.
3.2. Respirometry and soil temperature
CO2C emissions and soil temperature data at different soil management systems during the study period are given in Fig. 3. Annual average CO2C emissions (mol CO2 m 2 s 1) among different soil
management systems followed the order: FS (2.60) N ACS (2.09) N NR
(2.00). This is equivalent to an annual efux of 9.08; 7.91 and
7.57 Mg CCO2 ha1 year1, respectively. NR tended to has a higher capacity to reduce CO2C emissions than ACS and FS. A similar trend was
observed in the ACS and NR in its potential to reduce CO2C emissions.
FS tended to has higher CO2C emissions to the atmosphere. Mean soil
temperature was 21 C and 22.6 C for NR and ACS, respectively. FS
tended to present the highest mean soil temperature (26 C; Fig. 3b).
CO2C emissions and soil temperature dynamics were observed to be
similar seasonally. An overall trend of higher values in summer (January) and lower values in winter (July) (Fig. 3a and b) was recorded. Linear relationship and its parameters between CO2C emissions and soil
temperature are reported in Fig. 4 and Table 3. Q10 factor, which represents the percentage increase in emission for a 10 C increase in soil
temperature, was 3.45, 3.22 and 2.52 in NR, ACS and FS, respectively.
The B parameter was observed to be lower in FS (0.093), showing less
sensitivity to increases in soil temperature.
3.3. Moisture and microbial biomass C
Fig. 5 shows means of soil moisture, microbial biomass C, soluble
carbon, metabolic and microbial quotient of different soil management
systems. Annual averages of soil moisture tended to be higher in NR

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

19

Fig. 2. Mean values of total organic C (a), total N (b), C/N ratio (c), labile C (d), recalcitrant C (e) and bulk density (f) in different soil management systems and for different layers. Horizontal bars represent the standard error. NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system.

(0.17 m3 m3) and ACS (0.15 m3 m3) than in FS (0.12 m3 m3). The annual
microbial biomass C was observed to be higher in NR (232.71 mg kg1)
and ACS (189.22 mg kg1) than in FS (128.69 mg kg1), and similar
trends were also observed in case of soluble carbon. A trend of higher
metabolic quotient indicates that FS has a major level of disturbance
and energy demand (Fig. 5d) compared to the other soil management
systems for all study periods. Relationship between microbial biomass
C and total organic C (microbial quotient) is leaning to be higher in FS
(1.85%) than in ACS (0.95).

Table 2
Mean values of carbon and nitrogen stocks (C and N stocks) in Mg ha1 at 0100 cm layer
and probabilities after randomization tests comparing orthogonal contrasts among different soil management systems.

C stock
N stock

NR

ACS

FS

125.21
12.82

103.93
10.30

78.61
7.26

NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system.

3.4. Soil quality index

The selected variables (14 soil attributes previously mentioned)
were included in the PCA to determine soil quality index. The PCA generated 14 PCs. According to Kaiser criterion, the minimum number of
components to retain was equal to three as the eigenvalues started to
be lower than 1 at PC3 (Table 4). Therefore according to this criterion,
the rst three PCs should be kept. Three principal components (PC1, 2
and 3) have eigenvalues N 1.00 and explained 94% of the variance in
the data set (Table 4). Consequently, the rst three PCs were retained
to represent the original variability of the data-set. The other components gave a relatively small contribution to the variance. The PC1 had
seven highly weighted variables: total organic C, C and N stock, CO2C
emission, soil temperature, microbial biomass C and metabolic quotient.
The PC2 had one highly weighted variable: C/N ratio. The highly weighted variables for the PC3 included labile and soluble C.
A correlation matrix for the highly weighted variables under different PCs was run separately to nd out redundant variables within
each PC (Table 5). The highly weighted variables under PC1 were all signicantly correlated (excepted N stock). Soil CO2C emission, soil

20

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

Fig. 3. Mean values of CO2C emissions (a) and soil temperature (b) in different soil management systems. Vertical bars represent the standard error. NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system.

temperature and metabolic quotient were included in the minimum

data set, since these variables play an important role in C dynamics
among the selected agroecosystems. Under PC2, C/N ratio was included
in the minimum data set. Under PC3, both labile C and soluble C were
retained for the minimum data set because they were not correlated
(r = 0.322, p N 0.05). The indicators selected for the nal soil quality
index were soil CO2C emission, soil temperature, metabolic quotient,
C/N ratio, labile C and soluble C. The weights for selected variables
were determined by the percentage of variation in the data set explained by PC1, 2 and 3 (Table 4). The SQI equation was based on the
nal normalized PCA (full value for not correlated variable and divided
for correlated ones). The soil quality index (SQI) was computed as follows (Eq. (3)):
Normalized SQI 0:23SCO2 0:23Stem 0:23SQmet 0:17SCN
0:08SLabc 0:08SSolc =1:19Final SQI 0:19SCO2 C
0:19Stem 0:19SQmet 0:14SCN 0:06SLabc
0:06SSolc

where: CO2C = soil CO2C emission; temp = soil temperature;

Qmet = metabolic quotient; CN = C/N ratio; Labc = labile C; Solc =
soluble C, coefcients are the weighting factors and S is the score for
each variable.

Fig. 6 shows the SQI and the specic contribution of each indicator
towards the SQI for the different management systems. Overall, scored
values for all indicators were observed to be higher under NR and ACS
than in FS (SQI values 0.5, 0.48 and 0.31, respectively). Considering
the specic contribution of each score generated, the CO2C emission,
soil temperature and metabolic quotient had a signicant contribution
in the SQI for all selected sites (16, 27 and 32% in average, respectively).
Metabolic quotient had signicant contributions in the SQI (45.6%).
4. Discussion
Land management practices inuence the quantity, quality and distribution of soil organic carbon in agricultural systems (Pezarico et al.,
2013). The trend of total organic C near-surface in NR and ACS when
compared to FS is due to the continuous input of organic material provided by litterfall. The results show that ACS tends to increase C and N
stocks as compared to FS. Aboveground C in ACS ranged from 0.29 to
15.21 Mg ha 1 year 1 and from 30 to 300 Mg C ha 1 up to 1 m
depth in the soil (Nair et al., 2010). Soto-Pinto et al. (2010) reported signicant C accumulation in agroforestry coffee systems (50 Mg C ha1 in
average) in Mexico. The amount of biomass input and species diversity
in ACS is comparable to natural ecosystems, with higher potential to
storage of C and N than FS (Matos et al., 2011).
The results indicate that the dry season, with low moisture (Fig. 5a)
and soil temperature (Fig. 3b), decreases the rates of microbial biomass
activity (Fig. 5b). This pattern is more pronounced in the FS system. The
end of dry season and the beginning of rainy season (in October) promoted increases in soil temperature and moisture, contributing to increased CO2C emissions (Fig. 3a and b) as well as microorganism
activity in the soil (Fig. 5b). Liebig et al. (2013) reported that summer
months were characterized by signicantly higher CO2C emissions
(15.26 Mg CO2C ha1 year1), parallel to higher soil temperatures,
while spring and fall were similar (4.856.93 Mg CO2C ha1 year1).
It was observed that ACS reduced CO2C emissions in 1.93 Mg CO2
Table 3
Parameters of the model between CO2C emissions and soil temperature for and Q10 factor for the different soil management systems.
Management
systems
NR
ACS
FS

Fig. 4. Linear relationship related to log(CO2C) emissions and soil temperature, for native
rainforest (NR); agroforestry coffee system (ACS) and full sun coffee system (FS). n = 72.

Ln(CO2C emission) = A + (B Tsoil)

A

R2

Q10

1.946 0.489
1.937 0.601
1.466 0.609

0.124 0.023
0.117 0.027
0.093 0.023

0.546
0.445
0.390

0.381
0.911
0.717

3.456 0.171
3.222 0.194
2.522 0.142

N = 72, A and B: linear and angular coefcients, respectively; R: correlation coefcient; P:

signicance level. NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee
system.

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

21

Fig. 5. Mean values of soil moisture (a), microbial biomass C (b), soluble C (c), metabolic quotient (d) and microbial quotient (e) in different soil management systems. Vertical bars represent the standard error. NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system.

C ha1 year1 when compared to FS. This value (agroforestry versus

full sun) was lower than those reported by Hergoualc'h et al. (2012)
(10.76 Mg CO2C ha1 year1) in Costa Rica, due to agroforestry system's
characteristics. Noponen et al. (2013) also reported a positive C balance in
shaded coffee system (21.88 Mg CO2C ha1 year1) and a negative C
balance in full sun coffee system (0.13 Mg CO2C ha1 year1). Coffee
plantations occupy 452,527 ha in the state of Esprito Santo, which represents about 10.2% of the total land area. A very small segment of the total
area is currently under agroforestry coffee systems (~10%) (Sales et al.,
2013). If a transition from FS to ACS occurred, 785 Mg CO2C ha1 year1
would not be released to the atmosphere. This would be representative
at regional and global scales, once coffee production in Esprito
Santo is responsible for almost 20% of the world's production (Sales
et al., 2013).

ACS has higher capacity to decrease soil disturbance (greater aggregate stability), reduce soil temperature and increase water holding
capacity. Stable aggregates provide a physical protection of soil organic
matter and decrease the vulnerability to attack by microorganisms
in reduced tillage systems, consequently decreasing losses of C
(imansk, 2013; Thomazini et al., 2013). Due to organic material inputs
through litterfall and the mild climate provided by their canopies, agroforestry coffee systems create a higher soil moisture availability and
mild temperatures (Nair et al., 2008). The signicant positive correlation between soil CO2C emissions, moisture and temperature indicates
that organic matter decomposition processes are dependent on
water availability and soil temperature (Davidson and Janssens, 2006).
Liebig et al. (2013) reported that soil temperature was correlated with
CO2C emissions during the spring and fall, and with soil moisture

22

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

Table 4
Outcome of principal component analysis for the rst ve principal components (PC).
Principal components
Eigenvalue
Variability (%)
Cumulative %
Eigenvectors:
Total organic C
Total N
C/N ratio
Labile C
Recalcitrant C
C stock
N stock
CO2C emission
Soil temperature
Moisture
Microbial biomass C
Soluble C
Metabolic quotient
Microbial quotient

PC1

PC2

PC3

PC4

PC5

9.716a
69.401
69.401

2.403
17.166
86.567

1.155
8.248
94.815

0.448
3.197
98.012

0.238
1.701
99.713

0.285b
0.275
0.059
0.230
0.216
0.303
0.299
0.310
0.317
0.267
0.304
0.213
0.319
0.226

0.245
0.210
0.627c
0.299
0.473
0.103
0.141
0.075
0.027
0.108
0.001
0.141
0.010
0.348

0.219
0.367
0.131
0.478
0.009
0.118
0.187
0.044
0.057
0.423
0.023
0.508
0.011
0.283

0.035
0.050
0.056
0.112
0.015
0.365
0.075
0.309
0.166
0.149
0.426
0.646
0.007
0.311

0.198
0.107
0.014
0.023
0.200
0.024
0.364
0.042
0.132
0.494
0.268
0.333
0.163
0.551

Fig. 6. Soil quality index (SQI) and the individual contribution of each indicator towards
the soil quality index under different management systems. CO2C: soil CO2C emission;
Temp: soil temperature; Qmet: metabolic quotient; C/N: C/N ratio; Labc: labile C; Solc: soluble C; NR: native rainforest; ACS: agroforestry coffee system; FS: full sun coffee system.

a
Boldface eigenvalues correspond to the principal components examined for the soil
quality index.
b
Boldface eigenvectors are considered highly weighted.
c
Bold-underlined eigenvectors correspond to the indicators included in the minimum
data set.

during the summer. The accumulation of vegetation residues from

plants and trees acted as a physical barrier, reducing evapotranspiration, enhancing inltration and water holding capacity in NR and
ACS, as compared to FS (Fig. 5a). Thus, soil exposure promoted
higher soil temperatures in the following order: FS N ACS N NR. A 2 C increase in temperature is roughly countered by a concurrent 10%
decrease in soil moisture content (Leiros et al., 1999). In the
current study, results showed that CO2C emissions is leaning to be
higher in the FS, which tended to have less soil moisture. Despite this
general relationship, the effect of shade on temperature reduction is
more prominent than that of moisture increase, in terms of CO2C
mineralization.
Although the current research did not evaluate the C input, treatments that receive more C inputs are also reported with the lowest
CO2C emissions and the C stored in the soil is higher than that of FS systems (Makumba et al., 2007; Nair et al., 2010). This emphasizes the importance of ACS in sequestering C alongside natural rainforest systems.
Thus, results indicate that agroforestry coffee system was observed to
act more as a C sink than FS. In the context of relatively food insecure
farmers, agroforestry offers a solution by combining food production
and biomass for energy (Nair et al., 2009). Benets that ACS provide in
addition to C sequestration are early generation of income from
annual and semi-perennial intercrops and improved nutritional
quality of food. In addition, there is less risk in practicing agroforestry
than monocropping with respect to climatic disasters, market
uctuations, and pest/disease attacks (Saha et al., 2011). All these

improvements are associated with socioeconomic aspects and biodiversity conservation.

Results suggest that the microbial biomass C tended to be more
immobilized in FS than in NR and ACS. However, metabolic quotient
values suggest a high C demand in FS and an energy transfer for cell
maintenance instead of growth (Anderson and Domsch, 2010). Therefore, a higher proportion of microbial biomass C is being lost as CO2C
(Fig. 3a) instead of being incorporated into the soil in FS. NR and ACS
tended to have higher sensibility to CO2C emissions when soil temperature increases, when compared to the Q10 values in FS (Table 3). In this
context, soil organic matter attributes are largely responsible to that response in soil temperature increases. Chemical theory predicts that labile forms of organic matter should be more sensitive to changes in
soil temperature than recalcitrant forms. This leads to a reduction in organic matter mineralization and CO2C emissions (Anderson and
Domsch, 2010; Stockmann et al., 2013). However, there was no correlation between CO2C emissions, labile, recalcitrant and soluble C in the
current study. Labile and soluble C was observed to be higher up to
20 cm depth in NR (13.03 g kg 1 and 168.88 mg kg1, respectively)
and in ACS (10.60 g kg 1 and 151.83 mg kg 1, respectively). In this
case, Q10 values indicate a possible trend, where NR and ACS are dynamic systems and organic C is being cycled faster compared to FS.
These results show that in a climate change scenario, with increases in
soil temperature, higher labile and soluble C contents will be rapidly
mineralized by microorganisms in these systems. These results further
emphasize that if the NR or ACS is deforested, high amounts of C will
be rapidly mineralized and emitted to the atmosphere. Fresh organic
matter input may induce microbial growth and an increase in the production of enzymes leading to an acceleration of soil organic matter
mineralization (Souza et al., 2012).

Table 5
Correlation matrix for the highly weighted variables under the rst three principal components.

Toc
C/N
Labc
Estc
Estn
CO2C
Temp
Biom
Solc
Qmet

Toc

C/N

Labc

Estc

Estn

CO2C

Temp

Biom

Solc

0.499
0.582
0.743
0.680
0.831
0.852
0.844
0.404
0.897

0.392
0.042
0.014
0.052
0.152
0.187
0.030
0.200

0.662
0.661
0.790
0.687
0.645
0.325
0.700

0.949
0.873
0.976
0.969
0.629
0.935

0.905
0.937
0.882
0.727
0.915

0.935
0.856
0.726
0.960

0.980
0.661
0.989

0.541
0.955

0.678

Qmet

Toc: total organic C; C/N: C/N ratio; Labc: labile C; Estc: C stock; Estn: N stock; CO2C: soil CO2C emission; Temp: soil temperature; Biom: microbial biomass C; Solc: soluble C; Qmet:
metabolic quotient. Values in bold are different from 0 with a signicance level = 0.05 (Pearson correlation).

A. Thomazini et al. / Geoderma Regional 5 (2015) 1524

Regional climate characteristics exert great inuence on Q10 estimated values. Epron et al. (1999) reported that the increase in Q10
values of soil respiration is higher at low temperatures than at high temperatures. Kirschbaum (1995) obtained an even greater range of Q10
from 4.5 at 20 C to 2.5 at 30 C. Since the current study reports soil temperature ranged from 19 to 22 C (NR) and 20 to 24 C (ACS) compared
to 24.5 to 27.5 C (FS), higher Q10 values were recorded in NR and ACS.
In agricultural systems with stable organic matter, mainly due chemical
protection by electrostatic surfaces and physical by aggregation, temperature sensitivity is lower (Chen and Tian, 2005). In this context, increases in soil temperature will not affect the mineralization and C
release to the atmosphere (Davidson and Janssens, 2006). We observed
that ACS also reduces soil temperature through shading by canopies and
litter. This effect should be taken into account to take full advantage of
this system in policies and programs for climate change mitigation
and adaptation.
According to the principal component loading matrix (Table 4), the
rst highly weighted variable group implies that PC1 is mainly associated with soil C pools and its dynamics (i.e., soil temperature acting as a
regulatory factor and metabolic quotient as a C storing indicator). In
the PC2, highly weighted variable suggests that this component is mainly related with soil mineralization process. The highly weighted
variables in the third component imply that it is mainly associated
with labile forms of organic C. In the present study, soil indicators
selected by PCA (soil CO2C emission, soil temperature, metabolic quotient, C/N ratio, labile and soluble C) are considered the most critical indicators for expressing the overall health of the soil and the subsequent
response to the management. In addition, soil CO2C emission, soil temperature, and metabolic quotient are the most important indicators for
soil quality in the Atlantic Rainforest Biome, since they gave the highest
average contribution towards the SQI. The SQI of 0.48 for ACS indicates
that while some effects of this system on soil quality are not ideal, they
are overall better than the FS, which had SQI of 0.31. Thus, through soil
quality assessment, results clearly show that management developed in
the ACS provides the soil to fulll some important functions, as reducing
soil disturbance and increasing C storage. Although the soil quality
index presented in this study used information from a narrow
timeframe, it could easily be used to more fully assess soil-quality dynamics in the Atlantic Rainforest Biome.

5. Conclusions
Soil management in the agroforestry coffee system improves soil
quality, according to the soil quality index calculated. Management
practices in the agroforestry coffee system provide a more efcient metabolism of C indicated by low metabolic quotient values. Thus, more C
is incorporated into the soil by microbial biomass C and the system is
less vulnerable to loss as CO2C emissions, unlike full sun coffee system,
which tended to have greater soil organic matter losses. The lack of vegetation residues on the soil surface in the full sun coffee system resulted
in increases in soil temperature, accelerated mineralization and reduction of total C and N stocks, contributing to higher CO2C emissions.
Considering the future climate change scenarios, there is a tendency
of incrementing on soil temperature and microorganism activity, which
contribute to an increase in soil respiration and C storing in labile C fractions in agroforestry coffee system in the Atlantic Rainforest Biome. This
further emphasizes the importance of the conservation of tree biomass
in established forest and agroforestry systems, and the avoidance of
practices that reduce the stocks of soil organic matter.
Based on the soil quality index calculated, soil CO2C emission, soil
temperature and metabolic quotient would be the most effective tools
for assessing the effect of management on soil quality. Also, the soil
quality index obtained was able to synthesize the complex information
contained in large multivariate data-sets. Therefore, it would be useful
for application at regional and national scales in programs of assessing

23

the effect of management/tree planting recovery or maintenance of

soil quality.
Acknowledgments
The authors thank the farmers for the work in partnership, the
Brazilian sponsors CAPES (Coordination of Improvement of Personal
Higher Education), CNPq (National Counsel of Technological and Scientic Development), FAPES (Foundation for Research Support of the
State of Esprito Santo) for granting nancial support and scholarships.
Appendix A. Supplementary data
Supplementary data associated with this article can be found in the
online version, at doi: http://dx.doi.org/10.1016/j.geodrs.2015.02.003.
These data include Google map of the most important areas described
in this article.
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