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Notaro et al. Soil microbial activity in agroforestry systems
87
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
Scientia Agricola
ABSTRACT: Agroforestry systems are an alternative option for sustainable production manage-
ment. These systems contain trees that absorb nutrients from deeper layers of the soil and leaf
litter that help improve the soil quality of the rough terrain in high altitude areas, which are areas
extremely susceptible to environmental degradation. The aim of this study was to characterize
the stock and nutrients in litter, soil activity and the population of microorganisms in coffee (Cof-
fea arabica L.) plantations under high altitude agroforestry systems in the semi-arid region of the
state of Pernambuco, Brazil. Samples were collected from the surface litter together with soil
samples taken at two depths (0-10 and 10-20 cm) from areas each subject to one of the follow-
ing four treatments: agroforestry system (AS), native forest (NF), biodynamic system (BS) and
coffee control (CT).The coffee plantation had been abandoned for nearly 15 years and, although
there had been no management or harvesting, still contained productive coffee plants. The ac-
cumulation of litter and mean nutrient content of the litter, the soil nutrient content, microbial
biomass carbon, total carbon, total nitrogen, C/N ratio, basal respiration, microbial quotient,
metabolic quotient and microbial populations (total bacteria, fl uorescent bacteria group, total
fungi and Trichoderma spp.) were all analyzed. The systems that were exposed to human inter-
vention (AS and BS) differed in their chemical attributes and contained higher levels of nutrients
when compared to NF and CT. BS for coffee production at high altitude can be used as a sustain-
able alternative in the high altitude zones of the semi-arid region in Brazil, which is an area that
is highly susceptible to environmental degradation.
Introduction
Coffee (Coffea spp.) is the most popular and most
consumed drink in the world (Selvamurugan et al.,
2010). Coffee is the primary commodity produced by
Brazil, where the majority of the coffee crop is produced
under monoculture systems and full sun. However, this
management practice reduces fertility, organic matter
and soil yield.
Agricultural practices based on ecological prin-
ciples (such as agroforestry) can combine production
with conservation of the remaining fragments of natural
forests (Buck et al., 2006). Agroforestry is based on prin-
ciples of diversifi cation, recycling, biological processes
and the imitation of natural habitats (Lernoud, 2004), of-
fering multiple techniques such as windbreak systems,
silvopastoral, and intercropping / alley cropping, among
other variations. Agroforestry can be an interesting al-
ternative for environmental, social and economic devel-
opment because it does not pollute the environment or
people directly and indirectly involved, and can gener-
ate additional income for the farmer.
The litter deposition in these agroforestry systems
is responsible for signifi cant additions to the contents
of organic matter (OM) of the soil (Hergoualc’ha et al.,
2012; Tumwebaze et al., 2012), which might be equiva-
lent to a forest that has experienced no human interfer-
ence (Lima et al., 2010). Many benefi ts have been at-
tributed to the use of agroforestry systems such as: (i)
improvement of the nutrient cycle (Nair et al., 1999); (ii)
increase in microbial populations and soil OM contents
(Chander et al., 1998; Souza et al., 2012); (iii) reduction
of the weed population (Beer et al., 1998; Sileshi et al.,
2007); (iv) reduction of nutrient losses caused by turn-
ing biomass (Montagnini and Nair, 2004; Mutual et al.,
2005); (v) reduction of runoff; (vi) increase of water in-
fi ltration (Barreto et al., 2011); and (vii) reduction of ero-
sion and nutrient input.
Because biological indicators are extremely sensi-
tive when attempting to detect changes in soil quality,
there has been a growing interest in studying and com-
paring the microbial attributes in agroforestry systems
to other production systems (Paudel et al., 2012). The
aim of this study was to characterize the stock and nutri-
ent in litter, soil activity and population of microorgan-
isms from coffee plantations at high altitude in different
agroforestry systems in the semi-arid region of the state
of Pernambuco, Brazil.
Materials and Methods
This study was conducted on agroforestry coffee
growing systems and a native forest in the semi-arid re-
gion of Taquaritinga do Norte, in the state of Pernambuco,
Brazil (07º54'17” S, 36º05'32" W). The region’s climate is
classifi ed as CSA type, with an average temperature of 18
ºC at an altitude of 900 m. All areas were similar in terms
of climate, soil type, topography and altitude.
Three types of coffee production used in agro-
forestry coffee producing systems (agroforestry, biody-
Received June 07, 2012
Accepted November 14, 2013
Federal Rural University of Pernambuco/Academic Unit of
Garanhuns, Av. Bom Pastor, s/n − 55292-270 − Garanhuns,
PE − Brazil.
*Corresponding author <gpduda@gmail.com>
Edited by: José Miguel Reichert / Luís Reynaldo Ferracciú
Alleoni
Agroforestry systems, nutrients in litter and microbial activity in soils cultivated with
Krystal de Alcantara Notaro, Erika Valente de Medeiros, Gustavo Pereira Duda*, Aline Oliveira Silva, Patrícia Maia de Moura
coffee at high altitude
88
Notaro et al. Soil microbial activity in agroforestry systems
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
namic and coffee control) were found in the various ar-
eas, together with a native forest, that was next to the
production fi elds which constituted a control area. The
treatments were as follows:
Agroforestry or silvopastoral system (AS): This area
contained 25 ha of coffee that had been cultivated in
shade since 1986. Prior to this date, the cultivation of
coffee had been the conventional type. The variety is
the Coffea arabica typica, with a spacing of 2.5 m be-
tween plants. The plants responsible for the shading are
banana (Musa paradisiaca), cashew nuts (Anacardium
occidentale), legumes (Leucaena leucocephala) and trees
native to the region, mostly Jurema (Mimosa tenuifl ora).
Some animals, such as free-roaming goats, are raised in
the production fi elds.
Native forest (NF): This area was investigated for com-
parative purposes and served as the control treatment.
The area was composed of deciduous forest and old
trees with a closed canopy, high litter deposition. Ad-
ditionally, the area was wet,extremely rugged and was
free from human intervention.
Biodynamic system (BS): This area contained 8 ha
of coffee in full production. It was shaded with fruit
trees, such as cashew, banana and other plants, that
are indigenous to Ingazeira (Inga cylindrica). The area
is fl atter than the other areas, had more closed canopy,
and a larger amount of litter deposition. This area had
also been subjected to constant application of cattle
manure.
Control (CT): This relatively smooth area of the coffee
plantation had been abandoned for nearly 15 years and,
although there had been no management or harvesting,
still contained productive coffee plants.
In each environment (AS, NF, BS, CT), three pre-
scaled sub-areas of 100 m2 were selected, one for each
repetition. In February 2010, eight soil and litter simple
sub-samples were collected for each replicate and homog-
enized to form a composite sample for repetition. The litter
samples were collected from the surface of the soil using a
square of PVC that was 0.20 × 0.20 cm at each sampling
point to form a composite sample. During the same sam-
pling, the soil samples were collected at 0-10 and 10-20 cm
depth. The samples were maintained at their fi eld moist
condition and stored at 4 ºC until analyzed.
The litter samples were cleaned and then dried in
an oven at 65 °C for 48 h. The samples were sieved in
a 2 mm mesh. For the determination of N, P, K, Ca and
Mg, 0.5 g of dry matter from each sample was dried and
digested in a microwave oven using a mixture of nitric
acid / hydrochloric acid (Embrapa, 2009). In the extracts,
K was determined photometrically, Ca and Mg were de-
termined by atomic absorption, and P was determined
by colorimetry (Embrapa, 2009). Total organic carbon
(TOC) and total nitrogen (TN) were determined through
combustion at a temperature of 925 °C in a CHNS-O
elemental analyzer (Perkin Elmer PE-2400). To perform
the analysis, 1 to 2 mg of litter which had already been
previously dried and sieved were used. The reference
standard used was acetonitrile (C = 71 %, H = 7 %, N
= 10 %).
The soil samples were covered and set aside to
dry. After drying, the samples were passed through a
sieve of 2 mm mesh for chemical characterization in ac-
cordance with the methodology recommended by Em-
brapa (2009). The pH was determined in water at the
ratio 1:2.5 soil: solution, the available P was determined
by colorimetry after extraction with Mehlich-I, the ex-
changeable K was determined by fl ame photometry after
extraction with Mehlich-I, and the exchangeable Ca, Mg
and Al were extracted with 1 M KCl and determined by
titrimetry as prescribed by Embrapa (2009).
To determine the microbial carbon biomass
(MCB), the samples were submitted to an irradiation
process. For this measurement, we adopted the method
described by Vance et al. (1987) using 0.5 M K2SO4 as
the extract and placed 80 mL of 0.5 M K2SO4 in 20 g of
soil moisture content. The carbon in the K2SO4 extracts
was determined by colorimetry (Bartlett and Ross, 1988).
The basal respiration (BRS) of the microbial pop-
ulation of the soil was determined by quantifying the
carbon dioxide (CO2) released in the process of micro-
bial respiration (CO2 evolution) using the alkali adsorp-
tion method with adjustments for the humidity of the
soil samples to 60 % of its fi eld capacity (Anderson and
Domsch, 1985). Aliquots of 30 g were drawn from the
soil samples and placed in individual airtight containers,
where the CO2 produced was captured by 0.5 M NaOH.
After 72 h of incubation, the amount of CO2 was quanti-
fi ed by titration with 0.25 M HCl, and the addition of
barium chloride solution (0.05 M BaCl2) to the NaOH so-
lution, using phenolphthalein diluted in 100 mL of ethyl
alcohol (95 % v/v) as an indicator.
Total organic carbon (TOC) and total nitrogen
(NT) were determined using the elemental analyzer de-
scribed above. The metabolic quotient (qCO2) was cal-
culated as the ratio between the BRS / CMB (Anderson
and Domsch, 1993), and the microbial quotient (qMIC)
was calculated using the CMB / TOC ratio, according to
Sparling (1997). The samples underwent serial dilution
to detect the microorganism populations of total bacteria
(TB), fl uorescent group bacteria (FGB), total fungi (TF)
and Trichoderma spp. (TRI) in the soil. Plates were incu-
bated at 25 °C with a photoperiod of 12 h. The bacterial
populations (TB and FGB) were evaluated after 24 h of
incubation, whereas the TF was evaluated after 48 h of
incubation.
The TRI populations were evaluated after 120 h of
incubation. In each plate, colonies were quantifi ed using
a colony counter. The number of microorganisms were
used in the following formula: Population = number of
colonies × dilution factor × 10 with the latter represent-
Notaro et al. Soil microbial activity in agroforestry systems
89
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
ing the adjustment factor for plating 1 mL of suspen-
sion per plate and expressed as colony forming units per
gram of soil (CFU g−1 soil)
Data were submitted to analysis of variance and
means were compared by Tukey test (p < 0.05), and
principal component analysis (PCA). The original vari-
ables with the highest weight (loadings) in the linear
combination of the fi rst principal components were con-
sidered the most important. Thus, the data from the mi-
crobiological and chemical soil attributes of the four ar-
eas were compared using principal components analysis
and the Statsoft data analysis software system, version
7.0 (Statistica, 2011). This analysis yielded a group that
was reduced to two principal components (factors 1 and
2), identifi ed in a two-dimensional graph, containing the
original information.
Results
The areas with NF, CT and BS presented similar
litter deposition values, while the AS treatment had the
lowest litter value (Table 1). The content of Ca in the lit-
ter of the AS and NF treatments was higher than in the
other treatments (Table 1). The content of K in the litter
from NF was the lowest in relation to other treatments.
The content of Mg in the litter from CT, NF and BS treat-
ments are similar, except in areas under AS litter which
d the lowest content of Mg in litter. The CT litter had
lower values for P. The litter from the coffee plantations
in BS and AS had higher values of P.
The content of TOC and TN were not different (p
< 0.05), indicating that the areas used for the produc-
tion of coffee in agroforestry systems at high altitude
showed TOC and TN in quantities similar to the native
forest (NF). The C/N litter ratio obtained for the AS and
BS systems were similar to NF (Table 1). The pH of the
soil from the different coffee producing agroforestry sys-
tems had values above 5. The only exception was the soil
from NF, which had values of 4.7 and 4.3 at depths of
0-10 cm and 10-20 cm, respectively. The soils from areas
subjected to AS, BS and CT treatments indicated similar
pH values (Table 2).
When comparing areas, the lowest content of Al
was found in soils from NF treatment. The soils collect-
ed from AS had higher levels of Na, K, Ca and P in the
surface layer of the soil. There was a decrease in the Ca
content in relation to depth Except for the soil in which
the CT from both depths did not differ in content of Ca,
the fi rst depth demonstrated the highest levels (Table 2).
In AS soils, the P content in the fi rst depth found in the
soils was 62 % higher than the level found in NF, which
was considered the control treatment. With the excep-
tion of the AS area, the other areas demonstrated low
values of P. This fi nding indicates the need to add this
element as a supplement to meet the demands of the
coffee plants.
The lowest levels of TOC were observed in the
area with CT soil at 0-10 cm depth. Reduced TOC con-
centrations were observed in CT and AS soils at 10-20
cm. No differences (p < 0.05) were found for the TN
variable between study areas when the depth was 0-10
cm. However, at a depth of 10-20 cm lower values of TN
were observed in soils from areas with CT and AS (Table
2). There was a difference between the C/N ratio of soils
in relation to the areas. The lower C/N ratio was found
in the CT soil system at both depths, while the highest
ratios were found in soils under NF and BS.
High values of the basal respiration of soil (BRS)
and microbial carbon biomass (MCB) were observed
for the soil covered with NF followed by BS (Table 3).
The values in NF were followed by the values in BS, AS
and CT. The highest values of BRS were also observed
in the surface soil. For MCB, only the soil covered with
NF and AS contained higher values of this attribute in
the surface soil (Table 3). Higher qCO2 were observed
in the NF and BS soils. The area with CT had the lowest
qCO2 value. The lowest qMIC was found in BS soils at
0-10cm depth, differing from other areas in which they
were similar. These results show that in BS soils there
is a lower microbial activity, as observed for the MCB
and qCO2.
TB and TRI population densities at the depth of
0-10 cm were higher in the soil from the coffee planta-
tions in the BS system, with averages of 8.1 × 106 and 3.7
× 105 CFU g−1 soil (Table 3). The soils of the CT and BS
systems presented similar populations of TB at 0-10 cm
depth. High variability was observed in the TF popula-
tions, and the treatment indicated a lower population of
these microorganisms in the BS soil and a larger popu-
lation in the NF treatment. Compared to the 10-20 cm
Table 1 − Yield and nutrient means content of the litter from high altitude coffee producing agroforestry systems in the semi-arid region of
Pernambuco, Brazil.
Treatments Litter Ca K Mg P TOC TN C/N
t ha−1 ------------------------------------------------------------------------------------------ kg ha−1 ------------------------------------------------------------------------------------------
AS 13.7 b 68.0 a 182.9 a 21.7 b 7.2 a 4769.0 a 299.3 a 16.1 b
NF 21.5 a 67.8 a 126.0 b 52.6 a 3.4 b 4841.3 a 332.0 a 14.5 b
BS 17.9 a 52.0 b 174.5 a 53.5 a 5.2 a 4628.0 a 294.0 a 15.7 b
CT 19.3 a 58.9 b 202.3 a 57.9 a 2.0 b 5906.6 a 246.0 a 23.5 a
CV (%) 10 10 16 13 35 23 12 17
AS = Agroforestry system; NF = Native forest; BS = Biodynamic system; CT = Control; TOC = Total organic carbon; TN = Total nitrogen; Values with the same letters
in the column are not different (Tukey’s test, p < 0.05).
90
Notaro et al. Soil microbial activity in agroforestry systems
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
depth, there was a decrease in the populations of TF and
BFG at 0-10 cm depth (Table 3).
The correlation matrix of biological and chemical
variables of soils under different cropping systems of
organic coffee at altitude showed high signifi cant cor-
relation coeffi cients (Table 4). There was increased mi-
crobial activity (BRS) with increased total carbon levels.
The aluminum levels infl uenced BRS, MCB and TF at
0-10 cm depth negatively.
To make a distinction between the treatments,
principal components were generated (Factor 1 and Fac-
tor 2) for the chemical (Na, P and pH) and microbial
attributes of the soil (TOC, MCB, TB, TF, and FGB) at
depths of 0-10 cm and 10-20 cm. Diagrams were gener-
ated for the projection vectors to demonstrate the soil
attributes that most infl uence the distinction between
the types of shade coffee production in agroforestry sys-
tems. Moreover, sorting diagrams that distinguished the
three groups of treatments (as confi rmed at two depths)
were plotted from the relationship between these com-
ponents (Figures 1B and 1D).
The PCA considered the fi rst two factors with a
cumulative value of 72 % for the chemical and microbial
attributes of the soil at a depth of 0-10 cm and 87 % at
a depth of 10-20 cm. For the data from a depth of 0-10
cm,factor 1 explained 42 % of the total variation of the
microbiological and chemical attributes. The variables
TB, MCB, TF, Na and P, which had the highest correla-
tion coeffi cients (Table 5), are considered the most sensi-
tive for distinguishing the types of agroforestry systems
used in coffee production. However, these variables can
also be observed in the vector diagram, where the vari-
ables are closer to the axis of this factor (Figure 1A).
32 % of the factor 2 variance was explained by the
variables FGB, pH and TOC indicating the highest cor-
relations with this factor (Figure 1A and Table 5). At the
10-20 cm depth, the variables that correlated signifi cant-
ly with factor 1 were TF, FGB, Na, TB and pH, which
Table 2 − Soil nutrients content from high altitude coffee producing
agroforestry systems in the semi-arid region of Pernambuco,
Brazil.
Depth
(cm)
Systems
AS NF BS CT
pH (H2O 1:2.5)
0-10 5.7 aA 4.7 bA 5.8 aA 5.5 aA
10-20 6.0 aA 4.3 bA 5.6 aA 5.0 bA
Al mmolc dm−3
0-10 0.8 aA 0.5 bA 0.9 aA 0.85 aA
10-20 0.8 aA 0.9 aA 0.8 aA 0.7 aA
Na mmolc dm−3
0-10 1.9 aA 1.7 bA 1.5 bA 1.5 bA
10-20 1.7 bB 1.8 aA 1.4 dA 1.5 cA
K mmolc dm−3
0-10 1.7 aA 1.2 cA 1.5 bA 1.1 cA
10-20 1.0 aB 0.6 bB 1.3 aA 0. 8 bA
Ca mmolc dm−3
0-10 43.3 aA 20.0 bA 47.5 aA 10.0 bA
10-20 30.0 aA 10.0 bA 30.0 aB 10.0 bA
Mg mmolc dm−3
0-10 20.0 bA 10.0 bA 40.0 aA 20.0 bA
10-20 20.0 aA 10.0 bA 23.3 aB 10.0 bB
P mg dm−3
0-10 24.0 aA 5.0 cA 9.0 bA 5.00 cA
10-20 22.6 aA 5.0 cA 11.0 bA 5.1 cA
TOC g kg−1
0-10 34.2 aA 42.7 aA 45.6 aA 21.1 bA
10-20 23.3 bA 44.7 aA 40.5 aA 19.8 bA
TN g kg−1
4.7 aA 5.2 aA 5.6 aA 5.2 aA
3.9 bA 5.8 aA 5.3 aA 3.9 bA
C/N
0-10 6.8 aA 8.02 aA 8.09 aA 5.05 bA
10-20 5.8 bA 7.69 aA 7.52 aA 5.1 bA
AS = Agroforestry system; NF = Native forest; BS = Biodynamic system; CT
= Control. Coeffi cients of variation: pH = 9 %; Al = 16 %; Na = 4 %; K = 9 %;
Ca = 13 %; Mg = 14 %; P = 15 %; TOC (Total organic carbon) = 30 %; TN
(Total nitrogen) = 17 %; C/N = 15 %. Values with the same capital letter in the
column and lowercase letter in row are not different (Tukey’s test, p < 0.05).
Table 3 − Biological indicators of soil quality from high altitude
coffee producing agroforestry systems in in semi-arid region of
Pernambuco, Brazil.
Depth
(cm)
Systems
AS NF BS CT
BRS (mg C – CO2 kg−1 of soil h−1)
0-10 29.2 cA 59.4 aA 45.3 bA 23.6 cA
10-20 19.7 bA 53.8 aA 42.7 aA 17.8 bA
MCB (mg kg−1)
0-10 251 bA 358 aA 284 bA 242 bB
10-20 199 bB 212 bB 315 aA 293 aA
qCO2 (mg C – CO2 g−1 MCB - C h−1)
0-10 116.2 bA 166.0 aA 159.6 aA 97.4 bA
10-20 99.1 bA 133.7 aB 135.6 aA 60.9 cB
qMIC (%)
0-10 2.0 abA 1.7 abA 1.0 bA 2.3 aA
10-20 1.7 aA 1.0 aA 1.7 aA 1.0 aB
TB (x 106 CFU g−1 of soil)
0-10 3.2 bA 3.7 bA 8.1 aA 7.6 Aa
10-20 1.3 cB 0.7 cB 6.9 bB 8.8 Aa
TF (x 105 CFU g−1 of soil)
0-10 0.5 bA 1.09 aA 0.2 cA 0.3 Ca
10-20 0.1 bB 0.8 aB 0.1 bB 0.08 Bb
FGB (x 106 CFU g−1 of soil)
0-10 0.5 bA 0.7 aA 0.4 bA 0.3 Ba
10-20 0.3 aB 0.2 bA 0.1 bB 0.1 Bb
TRI (x 105 CFU g−1 of soil)
0-10 1.9 bA 0.5 cB 3.7 aA 1.7 Ba
10-20 0.2 bB 2.1 aA 0.8 bB 2.5 Aa
AS = Agroforestry system; NF = Native forest; BS = Biodynamic system and
CT = Control. Coeffi cients of variation BRS (basal respiration) = 5 %; MCB
(microbial carbon biomass) = 8 %; qCO2 (metabolic quotient) = 2 %; qMIC
(microbial quotient) = 8 %; TB (total bacteria) = 8 %; TF (total fungi) = 11
%; FGB (fl uorescent group bacteria) = 15 %; TRI (Trichoderma spp.) = 15 %.
Values with the same capital letter in the column and lowercase letter in the
row are not different (Tukey’s test, p < 0.05).
Notaro et al. Soil microbial activity in agroforestry systems
91
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
Table 4 − Correlation coeffi cients of microbiological and chemical attributes of the soils at a depth of 0-10 cm and 10-20 cm in high altitude
agroforestry systems in the semi-arid region of Pernambuco, Brazil.
Attributes 0-10 cm
BRS MCB qCO2qMIC TB TF FGB TRI
pH -0.55* -0.71* -0.41ns 0.13ns 0.24ns -0.55* 0.49ns 0.42ns
P -0.33ns -0.36ns -0.35ns 0.51* -0.46ns -0.21ns 0.74* 0.15ns
Al -0.52* -0.64* -0.43ns -0.07 ns 0.73* -0.88* 0.54* 0.75*
C 0.56* 0.29 0.61* -0.60* -0.11ns 0.22ns 0.04ns 0.20ns
N 0.44ns 0.15 0.53* -0.66* 0.01ns 0.14ns 0.02ns 0.25ns
10-20 cm
pH -0.62* 0.07ns -0.64* 0.29ns 0.16ns -0.77* 0.84* -0.68*
P -0.43ns -0.45ns -0.26ns -0.20ns -0.40ns -0.42ns 0.96* -0.90*
Al 0.42ns -0.26ns 0.49ns -0.41ns -0.39ns 0.43ns -0.20ns -0.10ns
C 0.89* 0.03ns 0.76* -0.65* -0.32ns 0.63* -0.47ns 0.01ns
N 0.88* 0.09ns 0.75* -0.58* -0.29ns 0.65* -0.55* 0.10ns
BRS = basal respiration; MCB = microbial carbon biomass; qCO2 = metabolic quotient and qMIC = microbial quotient; TB = total bacteria; TF = total fungi; FGB =
fl uorescent group bacteria and TRI = Trichoderma spp.; *signifi cant and ns = no signifi cant.
Figure 1 − Diagram of the vectors projection of the microbiological and chemical attributes of the soils at a depth of 0-10 cm (A) and 10-20 cm
(C) and the diagram ordination of the main components at a depth of 0-10 cm (B) and 10-20 cm (D) in the high altitude coffee agroforestry
systems in the semi-arid region of Pernambuco, Brazil. AS= Agroforestry system; NF = Native forest; BS = Biodynamic system; CT = Control;
MCB = microbial carbon biomass; TB = total bacteria, TF = total fungi, FGB = fl uorescent bacteria group and TOC = total organic carbon.
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Sci. Agric. v.71, n.2, p.87-95, March/April 2014
explained 50 %. For factor 2, the variables MCB, TOC
and P explained 37 % of the variation (Figure 1C).
At a depth of 0-10 cm, the variables MCB, TB and P
demonstrated positive correlation with factor 1 (Table 5),
which indicates that their average values increased from
left to right on the graph (Figure 1B) and that there was
negative correlation between the TF and Na variables.
Because the TB variable was positively correlated with
factor 2, their average values increased ascending from
the lower part of the graph and demonstrated negative
correlation with FGB and pH. At the 10-20 cm depth, the
variables that were highly correlated with factor 1 were
TF and C (the mean values increased when going from
left to right on the graph). MCB and TB (mean values
increased ascending the graph) were highly correlated
with factor 2 (Figure 1D).
The microbiological and chemical attributes used
in PCA showed differences between the types of organic
coffee production in agroforestry systems and native for-
est soil. Soils under BS and CT showed similar character-
istics and adjusted in the same quadrant at both 0-10 and
10-20 depth, differing from soils under NF.
Discussion
The stock of the litter was greatest in the NF, CT
and BS (Table 1). These results demonstrate the similar-
ity between the areas studied. Soils cultivated with high
altitude coffee under the shade of fruit trees or forest
species result in high additions of soil OM, making this
an important practice for maintaining high levels of soil
carbon, improving the soil fertility and soil microbial
activity. Hergoualc’ha et al. (2012) found higher carbon
stock using agroforestry systems with Inga trees to that
found in coffee monoculture. In general, the conver-
sion of forest systems to agricultural systems results in
a decline of litter and consequently soil organic carbon.
However, according to the results obtained by Tumwe-
baze et al. (2012) and this study, an agroforestry system
retains soil carbon stock.
The values of the litter are high when compared to
other studies. The litter stocks of this study are higher
than the litter stocks found by Lima et al. (2010), who,
analyzing areas with agroforestry systems six and ten
years after planting, in three-year old ecological based
systems, slash-and-burn agriculture and native forest, lo-
calized in Esperantina (03º54’ S; 42º14’ W), in the state
of Piauí, Brazil, and obtained an estimated annual litter
fall of 9.3 t ha−1 in agroforestry area after ten years. This
result is associated with the samples taken at the end of
the dry period, which provides a greater leaf fall because
of the physiological characteristics of the plant species in
these areas and the water defi cit (Martins and Rodrigues,
1999).
The content of the nutrients in the litter varied
among the types of coverage highlighting the area cov-
ered by BS and NF. In these areas, larger quantities of K,
N, Ca, Mg and P were found. Lima et al. (2010) observed
a higher contribution of N, P, K, Ca and Mg in an agro-
forestry system with ten years of implantation than in
the native forest. This contribution surpassed the values
of the native forest, which demonstrated the importance
of the agroforestry system. Leaves from the leguminous
trees could be the main source of organic N in the soil
(Mamani-Pati et al., 2012). However, a similar result was
not observed in this study. Compared to the other areas,
NF had higher values for the content of Ca, Mg and N.
The lowest values found were for K and P. Thus, all of
the areas demonstrated similar levels of nutrient accu-
mulation.
The low amount of P found in the litter is most
likely related to the mobility of the senescent tissues
when retranslocated to other parts of the plant. The lit-
ter can act as a sink of nutrients, which reduces its con-
tent in the leaves (Salisbury and Ross, 1992). In the litter
of all of the coffee production systems, the contents of
Ca, Mg, K and N, which can be a source of nutrients to
the culture after they are mineralized, were high. The
content of P in the litter was very low, which suggests
that this element is limiting in all of the systems evalu-
ated.
When compared to the other types of coverage,
the soil pH was lower in the soil covered with NF. This
lower pH might be associated with the failure to not use
a corrective for acidity in the soil covered with NF. This
result is confi rmed by the other areas that received a cor-
rective for acidity. These areas had higher pH values, as
well as higher values of Ca and Mg. As for K, the highest
levels observed might be associated with the application
of potassium fertilizers. As observed by Salgado et al.
(2006), the K, Ca and Mg in the soil covered with CT, BS
and AS are generally at levels suitable for the growth of
the plants as observed.
Only the land covered with the AS system had
adequate levels of P for plant growth, probably due to
Table 5 − Correlation coeffi cients of the principal components
analysis (factors 1 and 2) for the microbiological and chemical
attributes of the soils at a depth of 0-10 cm and 10-20 cm in
the high altitude agroforestry systems in the semi-arid region of
Pernambuco, Brazil.
Variables
Depth (cm)
0 - 10 10 - 20
Factor 1 Factor 2 Factor 1 Factor 2
MCB 0.81 0.21 0.05 0.94
TOC -0.56 0.82 -0.12 0.99
TB 0.94 -0.23 0.82 -0.57
TF -0.79 -0.38 -0.93 -0.34
FGB 0.28 -0.93 -0.93 0.06
Na -0.76 -0.19 -0.83 -0.50
pH -0.40 -0.86 0.65 -0.23
P 0.25 -0.06 0.05 0.94
Total variance (%) 42 32 37 50
MCB = microbial carbon biomass; TOC = total organic carbon; TB = total
bacteria; TF = total fungi; FGB = fl uorescent bacteria group.
Notaro et al. Soil microbial activity in agroforestry systems
93
Sci. Agric. v.71, n.2, p.87-95, March/April 2014
addition of P fertilizer. This result is again in agreement
with the fi ndings of Salgado et al. (2006). Generally, the
increased availability of P in agroforestry systems is as-
sociated with falling leaves of plants as observed by Ni-
gussie and Kissi (2012).
The low values of P in the soil and litter indicate
that this is the main limiting element in all of the sys-
tems evaluated. Thus, the soil provides little P to the
soil plants used in agroforestry systems. Additionally,
the plants in the agroforestry systems returned a low
litter result for P. Despite the low levels of available P in
the soil and litter, when the high levels of TOC and Ca
are taken into account, the occurrence of Al complexed
with organic molecules is possible because the levels of
organic P in these systems are high.
The content of TOC in the NF areas was not differ-
ent among AS, BS (Table 2). This was different from that
observed by Souza et al. (2012) in a coffee agroforestry
system in the Atlantic Rainforest biome, where the TOC
was higher in the soil in forests than in the soil under
coffee systems in Brazil. This result was also observed
in other studies that compared coffee producing agrofor-
estry systems in Indonesia (Hairiah et al., 2006) to the
content of TOC in Brazil (Maia et al., 2007).
Although the agroforestry systems are similar to
the NF in terms of altitude and the steepness of the ter-
rain and climatic conditions, an evaluation in this study
of the degree of similarity of the soil quality between
these hedges was not possible for TOC. This evaluation
was impossible because the canopy formation was in-
fl uenced by human involvement in the introduction of
fruit trees for commercial interests and because of the
introduction of coffee, which caused the amount of TOC
lost in relation to NF. NF also had a larger stock of litter,
which contributes to the greater stability of organic mat-
ter in undisturbed soil (Kaur et al., 2000).
The soil covered with NF that was evaluated at
both depths indicated higher values of BRS and MCB in
these areas. This fi nding indicates that there is a greater
loss of CO2 by microbial activity when compared to the
other areas. This loss of CO2 might be associated with
higher levels of TOC, which has a great infl uence on
microbial activity. Moreover, The MCB is vital for the
maintenance of soil quality because it is responsible
for the dynamics of the organic carbon (Dinesh et al.,
2003).
Losses in concentration of TOC, MCB, BRS, TF
and FGB in systems similar to NF (but which had been
subjected to human intervention as in the AS, BS and SB
systems) indicate that the detecting sensitivity of these
traits varies according to the type of use of soils (Sten-
berg, 1999). This diffi culty might occur because the soil
use type interferes with the dynamics of the soil organic
matter and the nutrient cycling processes in the decom-
position of soils (Acosta-Martinez et al., 2008).
The qCO2 values in the soils from the NF, BS and
AS areas were higher than in the CT area, which indi-
cates that the mineralization activity of the soil organic
carbon was higher in these areas. The higher values of
qCO2 indicate higher stress conditions and a higher loss
of CO2 per unit of microbial biomass in the systems. As
observed in the agricultural crops (Silva et al., 2007),
when compared to the native forestry, the higher levels
of qCO2 are generally observed in systems that suffer
from human intervention. However, in the case of this
study, the greater supply of organic matter might favor a
higher population of bacteria, which quickly attacks the
organic substrate and accelerates the process of biologi-
cal oxidation (Zibilske et al., 2002).
The variables most sensitive to the detection dif-
ferences in the treatments at a depth of 0-10 cm and
10-20 cm were MCB, TOC, TB, TF, FGB, Na, pH and P.
All of these variables were reduced to two factors (Factor
1 and Factor 2). Experiments with the fi rst two factors
have been performed in studies that evaluate the micro-
bial quality of the soil (García-Ruiz et al., 2008; Gardner
et al., 2011).
The importance of each variable in each princi-
pal component is indicated by the value of the modular
weight, which identifi es the variables that are correlated
with each principal component. Thus, the data from a
soil depth of 0-10 cm were the most important factor. For
factor 1, the order of importance was as follows: TB >
MCB > TF > Na > P. For factor 2, the order of impor-
tance was FGB > pH > TOC. At the 10-20 cm depth, the
most important variables for factor 1 were as follows:
TF = FGB > Na > TB > pH. For factor 2, the most
important variables were TOC > MCB = P. Many au-
thors have used principal components analysis and have
also highlighted the importance of the TOC and MCB
variables to explain the total variance of the treatments
(Wick et al., 1998).
The BS system is similar to NF when evaluating
production and nutrient content of litter. The systems
that were exposed to human intervention (AS and BS)
differed in their chemical attributes and had higher
levels of nutrients when compared to NF and CT. The
activity and microbial populations were higher in NF
soils, followed by BS soils indicating that a soil microbial
and chemical quality of BS is greater than or similar to
NF. Biodynamic systems for coffee production at high
altitude can be used as a sustainable alternative at high
altitude in the semiarid region of Pernambuco, Brazil,
which are areas that are highly susceptible to environ-
mental degradation.
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