Agroforest Syst (2014) 88:357–368
DOI 10.1007/s10457-014-9689-2
Short-term changes in the soil carbon stocks of young oil
palm-based agroforestry systems in the eastern Amazon
Walmir Ribeiro de Carvalho • Steel Silva Vasconcelos
Osvaldo Ryohei Kato • Carlos José Bispo Capela •
Débora Cristina Castellani
Received: 30 September 2013 / Accepted: 12 March 2014 / Published online: 25 March 2014
Ó Springer Science+Business Media Dordrecht 2014
Abstract The current expansion of the oil palm
(Elaeis guineensis Jacq.) in the Brazilian Amazon has
mainly occurred within smallholder agricultural and
degraded areas. Under the social and environmental
scenarios associated with these areas, oil palm-based
agroforestry systems represent a potentially sustainable
method of expanding the crop. The capacity of such
systems to store carbon (C) in the soil is an important
ecosystem service that is currently not well understood.
Here, we quantified the spatial variation of soil C stocks
in young (2.5-year-old) oil palm-based agroforestry
systems with contrasting species diversity (high vs.
low); both systems were compared with a *10-year-old
forest regrowth site and a 9-year-old traditional agro-
forestry system. The oil palm-based agroforestry system
consisted of series of double rows of oil palm and strips
of various herbaceous, shrub, and tree species. The
mean (±standard error) soil C stocks at 0–50 cm depth
W. R. de Carvalho
Programa de Pos-graduacao em Agronomia, Universidade
Federal Rural da Amazonia, Belem, PA, Brazil
S. S. Vasconcelos (&)  O. R. Kato
Embrapa Amazonia Oriental, Belem, PA, Brazil
e-mail: steel.vasconcelos@embrapa.br
C. J. B. Capela  D. C. Castellani
Natura Inovacao e Tecnologias de Produtos Ltda,
Cajamar, SP, Brazil
C. J. B. Capela
Universidade do Estado do Para, Belem, PA, Brazil
•
were significantly higher in the low (91.8 ± 3.1
Mg C ha-1) and high (87.6 ± 3.3 Mg C ha-1) species
diversity oil palm-based agroforestry systems than in the
forest regrowth (71.0 ± 2.4 Mg C ha-1) and tradi-
tional agroforestry (68.4 ± 4.9 Mg C ha-1) sites. In
general, no clear spatial pattern of soil C stocks could be
identified in the oil palm-based agroforestry systems.
The significant difference in soil carbon between the oil
palm area (under oil palm: 12.7 ± 2.3 Mg C ha-1 and
between oil palm: 10.6 ± 0.5 Mg C ha-1) and the strip
area (17.0 ± 1.4 Mg C ha-1) at 0–5 cm depth very
likely reflects the high input of organic fertilizer in the
strip area of the high species diversity oil palm-based
agroforestry system treatment. Overall, our results
indicate a high level of early net accumulation of soil
C in the oil palm-based agroforestry systems
(6.6–8.3 Mg C ha-1 year-1) that likely reflects the
combination of fire-free land preparation, organic
fertilization, and the input of plant residues from
pruning and weeding.
Keywords Brazilian Amazonia  Elaeis
guineensis  Regrowth forest  Slash-and-mulch
Introduction
Oil palm (Elaeis guineensis Jacq.) is one of the major
oilseed crops in Brazil and is an economically
important source of a plant oil that is widely used in
the food and cosmetic industries as well as biofuel
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production. Although Brazil ranks only 9th in the
world in palm oil production (USDA 2012), it is one of
the countries with the greatest potential to expand the
agricultural area of this crop because the soil and
climate conditions are suitable for the oil palm. To
meet the national demand, the Brazilian government
intends to expand the cultivated area of this oilseed
crop from approximately 120,000 hectares in 2011 to
more than one million hectares by 2020 (Brasil 2011).
Guidelines for the sustainable expansion of oil palm
cultivation rely on integrated production systems that
emphasize smallholder agriculture and cultivation in
degraded areas in the Amazon (Brasil 2011).
In the Amazon region, smallholder agriculture is
traditionally based on the slash-and-burn system with
alternating crop-fallow cycles (Denich et al. 2004).
This system usually reduces the productive capacity of
the soil when the recovery of soil carbon and nutrient
stocks in the fallow period is insufficient (Brady
1996); short fallow periods are increasingly common
in smallholder agricultural areas. Agroforestry sys-
tems (AFSs) have been identified as a sustainable
alternative form of land use for smallholder farmers in
the Amazon (Smith et al. 1995) owing to their
environmental, social, and economic advantages.
Thus, the cultivation of oil palm in AFSs represents
one potentially sustainable approach for crop expan-
sion in the Amazon. Such an alternative form of oil
palm cultivation would be particularly suited to
farmers in Tomé-Açu, a municipality in the State of
Pará, where smallholder agroforestry production is
common and economically relevant and an oil palm
expansion program has already been established. Such
a scenario raises concerns regarding the social effects
of transitioning fields and labor forces from agrofor-
estry to oil palm production and consequently requires
sustainable alternative forms of oil palm cultivation.
Another related concern is the potential for large
emissions of greenhouse gases resulting from the land-
use change to oil palm production, as has been
suggested for the state of Pará (Yui and Yeh 2013).
Thus, the potential for such increased emissions
presents an additional argument in favor of cultivating
oil palm in AFSs because of the mitigation potential of
these systems (Mutuo et al. 2005).
In the current context of climate change, agricul-
tural production systems that combine economically
viable yields with a high capacity for reducing
greenhouse gas emissions and/or enhancing soil
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Agroforest Syst (2014) 88:357–368
carbon accumulation are desirable. Thus, several
recent studies have focused on quantifying soil carbon
stocks in different agricultural production systems that
are often compared with non- or less-altered areas,
such as primary or old secondary forests (e.g., Frazão
et al. 2012; Desjardins et al. 2004) to infer land-use
change effects on soil carbon dynamics. In the
Amazon, few relevant studies have addressed the soil
carbon stocks in AFSs, and the spatial variation of soil
carbon stocks have not been well-studied for Amazo-
nian AFSs despite the potential role of species
diversity in affecting the soil carbon variability (Häger
2012). The spatial variability of soil carbon may also
be influenced by specific management practices, such
as the localized deposition of pruned leaves in oil palm
plantations (Law et al. 2009).
Here, we evaluated soil carbon stocks in two young
(2.5-year-old) oil palm-based AFSs that differed in
their species compositions. These systems were
established after fire-free land preparation using
slash-and-mulch technology (Denich et al. 2004),
which is a sustainable technology that promotes the
conservation of soil nutrients (Sommer et al. 2004) and
reduction of carbon dioxide-equivalent emissions to
the atmosphere (Davidson et al. 2008). We compared
both systems to a 10-year-old regrowth forest and a
9-year-old local traditional AFS. For the oil palm-
based AFSs, we also evaluated the spatial variability
of soil carbon stocks associated with the oil palm and
other species components. A better understanding of
the effects of oil palm-based AFSs on soil carbon
requires an understanding of the spatial and species
influence on soil carbon stocks.
We hypothesized that (1) the substitution of
regrowth forest with oil palm-based AFSs under
conservation management (fire-free land preparation
and input of organic fertilization sources) would not
negatively affect soil carbon stocks and (2) the high
species diversity would maintain higher soil C stocks
than the low species diversity oil palm-based AFSs.
Materials and methods
Study area
This study was conducted in the experimental area of
the project ‘‘Oil palm-based agroforestry in family
agriculture’’, which is a result of a partnership between
Agroforest Syst (2014) 88:357–368
Cooperativa Agrı́cola Mista de Tomé-Açu (CAMTA),
Natura Inovação, and Empresa Brasileira de Pesquisa
Agropecuária (Embrapa). The study area is located at
a smallholder farm (02°200 5900 S, 48°150 3600 W) in the
municipality of Tomé-Açu, Pará, eastern Amazonia.
In this municipality, medium to clayey textured
Oxisols are predominant (Baena and Falesi 1999). In
our study area, the soil texture varied from sandy loam
(0–10 cm depth) to sandy clay loam (10–30 cm
depth), and the texture was clayey at 30–50 cm depth.
The climate of the study area is hot and humid
and classified as Am according to the Köppen
classification system. According to data from 1985
to 2010 collected at the Embrapa Amazonia Oriental
meteorological station (02°380 S, 42°280 W, 45 masl),
the mean annual rainfall of Tomé-Açu was
2,440 mm, and 81 % of the annual rainfall occurred
between December and May. The average annual
temperature was 26.3 °C, monthly means varied
from 21.0 to 33.8 °C, and the average annual
sunshine was 2,372 h.
Experimental treatments
Prior to the experiment, the study area comprised an
approximately 10-year-old regrowth forest that had
grown after repeated slash-and-burn cycles for sub-
sistence agriculture (rice—Oryza sativa, cassava—
Manihot esculenta, maize—Zea mays, and cowpea—
Vigna unguiculata). In September and October of
2007, an approximately 6 ha fragment of the regrowth
forest with an aboveground dry biomass of
55.3 ± 0.9 Mg ha-1 (mean ± standard error) was
chopped and mulched. A mechanical chopper pulled
by tractor was used on four hectares, whereas in the
remaining area (2 ha), the vegetation was chopped by
hand using chainsaws and machetes. The chopped
vegetation was spread on the ground to form a mulch
layer. After land preparation, 1.3 Mg ha-1 of lime was
applied by hand to the soil surface.
In February of 2008, the intraspecific hybrid of oil
palm Tenera was planted as the main crop of two AFSs
that differed in species composition: (1) a low-
diversity system (OPlow) and (2) a high-diversity
system (OPhigh). In both systems, 13-month-old oil
palm seedlings were planted in double rows (spacing
7.5 9 9 m) interspersed with strips (width 15 m)
consisting of nine rows of herbaceous, shrub, and tree
species (Table 1).
359
A mixture of Arad reactive rock phosphate and
chaff charcoal (N 0.51 %; P 3.36 %; K 4.85 %; and
Mg 2.7 %) was placed (10 kg plant-1) in the planting
holes of the oil palm seedlings upon planting, whereas
the annual maintenance fertilization (sidedressing)
consisted of 8 kg of organic compost (N 1.2 %;
P 0.1 %; K2O 0.4 %; and C/N 46) per plant; the
organic compost contained peel, seed, and pulp
residues from a local fruit pulp industry. In 2009, the
sidedressing consisted of 40 kg of organic compost,
1.0 kg of bone meal (N 2 %; P2O5 20 %; K2O 0.12 %;
and C/N 9), and 1.0 kg of castor cake (N 5.44 %; P2O5
1.91 %; K2O 1.54 %; and C/N 10) per plant. The final
fertilization in 2010 prior to sampling supplied 0.3 kg
of reactive rock phosphate, 1 kg of bone meal, and two
applications of 50 kg of empty fruit bunches of oil
palm per plant each.
In the strips, tree seedlings were fertilized in the
same manner as the oil palm seedlings at planting. In
2008, the sidedressing consisted of 10 kg of chicken
manure (N 2.58 %; P2O5 2.77 %; K2O 2.31 %; and
C/N 7) and 20 kg of organic compost per plant. In the
other years, compost was not applied, and instead, the
biomass from the management of spontaneous vege-
tation and pruning of the fertilizing species (Musa
spp., Gliricidia sepium, Inga edulis, Tithonia diversi-
folia, M. esculenta, Canavalia ensiformis, Cajanus
cajan, and Crotalaria juncea) was used.
The AFS management consisted of removing the
vegetation from around the oil palm plants (3–5 times
per year), pruning old and damaged leaves (1–2 times
per year), and mowing between rows (3–4 times per
year). The resulting plant residues were distributed
beneath the crown of oil palm seedlings and under the
canopies of the other species.
The oil palm-based AFSs were compared with a
traditional agroforestry system in Tomé-Açu (TrAFS)
and a fragment of a 10-year-old regrowth forest
(RegFor); both areas were adjacent to the oil palm
systems (Fig. 1). The TrAFS site was established in
2003 to replace a 6-year-old black pepper (Piper
nigrum) monoculture using Theobroma cacao spaced
at 4 9 4 m, Euterpe oleracea spaced at 4 9 5 m, and
Swietenia macrophylla spaced at 16 9 16 m. In 2008,
the average canopy height in the 10-year-old regrowth
forest was 15 m, and the average density was
520 trees ha-1 (including only those trees with a
diameter at breast height [ 10 cm) (Izildinha Sousa,
personal communication). The most common species
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Table 1 Species planted in strips within low- and high-diversity oil palm-based agroforestry systems in the municipality of Tomé-
Açu, eastern Amazon, Brazil
Scientific name Family Propagation Propagules ha-1 Spacing (m) Species diversity
method
Low High

Cajanus cajan Fabaceae Seed 50 kg 0.25 9 1.50 9 9

Calophyllum brasiliensis Calophyllaceae Seedling 30 13.0 9 22.5 9
Canavalia ensiformis Fabaceae Seed 80 kg 0.30 9 0.30 9 9
Crotalaria juncea Fabaceae Seed 5 kg 0.25 9 0.25 9 9
Euterpe oleracea Arecaceae Seedling 125 6.0 9 6.0 9
Gliricidia sepium Fabaceae Cutting 280 3.0 9 12.0 9
Fabaceae 540 2.0 (between cuttings) 9
Inga edulis Euphorbiaceae Seedling 515 3.0 9 3.5 9 6.0 9
Fabaceae 540 3 9 5 9 17.5 9
Manihot esculenta Musaceae Cutting 600 1.0 9 1.0 9 3.0 9
Mucuna cinereum Arecaceae Seed 20 kg 0.50 9 1.0 9 9
Musa spp. Fabaceae Rhizome 595 3.0 9 3.0 9
Oenocarpus bacaba Bignoniaceae Seedling 85 4.5 9 22.5 9
Sclerolobium paniculatum Malvaceae Seedling 28 14.0 9 22.5 9
Tabebuia spp. Asteraceae Seedling 28 14.0 9 22.5 9
Theobroma cacao Arecaceae Seedling 300 3.0 9 3.5 9
Tithonia diversifolia Arecaceae Cutting 331 2.0 9 9

in the regrowth forest were Tapirira guianensis Aubl.,
Vismia guianensis Aubl., Inga alba Willd., and Apeiba
burchellii Sprague.
The treatments in our study were represented by the
oil palm-based AFSs, the local traditional AFS, and
the regrowth forest. Five plots were randomly estab-
lished in each treatment. For the oil palm-based AFSs,
each plot (22.5 9 18 m) included two rows of oil
palm and one strip; for the other treatments, plots
measured 20 9 20 m. The established plots were not
true treatment replications because other AFSs and
regrowth forest stands with the same age, manage-
ment, and soil conditions were not available. For this
reason, we considered our plots to be pseudo-repli-
cates, as have been used in many other related studies,
and acknowledge that this can represent a limitation of
our study (e.g., Frazão et al. 2012).
Soil sampling and analysis
In August 2010, soil samples were collected using
auger probes at five depths: 0–5, 5–10, 10–20, 20–30,
and 30–50 cm. We collected soil samples from several
different positions in the oil palm-based AFSs:
(a) under the oil palm canopy, (b) between oil palm
trees, and (c) within the strip area (Fig. 1). Soil from the
TrAFS and RegFor plots was sampled without a
defined spatial pattern. At each depth, three soil cores
from random sampling points were combined to
provide one composite sample per plot; for the oil
palm systems, we obtained five composite samples per
sampling position in each plot, and these composites
were combined for chemical analysis. All samples
were air-dried, ground, and passed through a 2-mm
sieve. Approximately 120 g of each sieved sample was
used for particle size and chemical analyses (Embrapa
1997). Soil pH was measured in water (1:2.5). Soil
exchangeable cations Ca2? and Mg2? were extracted
with 1 M KCL and analyzed using atomic absorption
spectrometry; K? was extracted with 0.05 M HCl and
analyzed using flame photometry. Phosphorus (P) con-
centration was extracted with Mehlich-l solution and
quantified using spectrophotometric method.
To determine the total concentration of C, approx-
imately 20 g of sieved soil was ground in a porcelain
mortar and passed through a 0.25-mm sieve. Approx-
imately 0.2000 g was then weighed to determine the C
concentration by dry combustion using a LECO CNS-
2000 elemental analyzer (Leco Corp., St. Joseph, MI).
The soil organic carbon stock (SOC, in Mg ha-1) for

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Agroforest Syst (2014) 88:357–368 361

Fig. 1 Experimental area A

layout (a) and soil sampling
locations and plant spacing RegFor
in the high-diversity (b) and
low-diversity oil palm-
based agroforestry systems
(c) in the eastern Amazon. In
a, OPlow low species
diversity oil palm-based
80 m
agroforestry system, OPhigh
high species diversity oil
palm-based agroforestry TrAFS
system, TrAFS local
traditional agroforestry 25 m
system, and RegFor OP high

regrowth forest. In b, c,
symbols represent sampling
locations (boxed cross), oil
palm plants (eight-spoked
asterisk), Musa sp. plants OP low
(black circle) and other 77 m
planted species (white
circle)
232 m road

B 1.5 m 1.5 m C 1.5 m

9m 9m

7.5 m 15 m 7.5 m 15 m

each layer was calculated using the following equa-
tion: SOC = (C 9 BD 9 th)/10, where C is the soil
organic carbon concentration (g kg-1), BD is the bulk
density of the sampled layer (depth) (kg dm-3), and th
is the layer thickness (cm).
In November of 2010, undisturbed samples were
collected to determine the soil bulk density. Four
trenches (length 120 cm, width 70 cm, depth 70 cm)
were dug per treatment, and soil samples were taken
using an extracting auger and Kopeck steel rings at 0–5,
5–10, 10–20, 20–30, and 30–50 cm from three walls of
each trench. The bulk density was determined by the
volumetric ring method (Embrapa 1997) and consisted
of drying the samples in an oven at 105 °C over 48 h.
The bulk density data were used to calculate the soil C
stocks.
To compare the oil palm-based AFSs with the
reference area (RegFor), all carbon stocks were calculated
based on the same weight of soil (Sisti et al. 2004).
Because the oil palm rows and strips occupied 35 and
65 % of the total area, respectively, carbon stocks were
calculated on an area-weighted basis (Frazão et al. 2012).
The net accumulation of soil carbon (DSOC) in the oil
palm systems was estimated using the following equa-
tion: DSOC = SOCagroforestry systems - SOCreference area.
For this calculation, we considered two assumptions:
(a) the soil C stock of the reference area represents the
baseline for our oil palm-based AFS plots, and (b) this
baseline level did not significantly vary during the
experiment (Neumann-Cosel et al. 2011).
Statistical analysis
A two-way analysis of variance (ANOVA) was used to
evaluate the effects of the oil palm systems and

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Table 2 Soil chemical characteristics at different depths in the OPhigh, respectively), 9-year-old traditional agroforestry sys-
treatment plots evaluated in 2.5-year-old low- and high- tem (TrAFS), and 10-year-old regrowth forest in Tomé-Açu
diversity oil palm-based agroforestry systems (OPlow and (RegFor), eastern Amazon
Treatment pH P K Ca2? Mg2? Al3?
mg dm-3 cmolc dm-3

0–5 cm
OPlow 6.11 ± 0.06 a 15.93 ± 5.85 a 129.53 ± 19.88 a 4.05 ± 0.34 ab 1.08 ± 0.05 ab 0.11 ± 0.01 B
OPhigh 5.81 ± 0.07 a 21.27 ± 8.19 a 70.13 ± 5.91 b 4.35 ± 0.29 a 1.34 ± 0.12 a 0.10 ± 0.00 B
TrAFS 5.86 ± 0.06 a 16.20 ± 4.49 a 29.80 ± 1.02 bc 2.76 ± 0.24 bc 0.94 ± 0.13 bc 0.10 ± 0.00 B
RegFor 5.08 ± 0.11 b 3.00 ± 1.00 b 21.80 ± 1.02 c 2.10 ± 0.40 c 0.68 ± 0.07 c 0.48 ± 0.14 A
5–10 cm
OPlow 6.05 ± 0.12 a 11.67 ± 5.20 a 105.13 ± 11.35 a 3.21 ± 0.38 a 0.93 ± 0.04 a 0.13 ± 0.02 B
OPhigh 5.77 ± 0.10 ab 12.67 ± 4.46 a 51.00 ± 5.24 b 3.45 ± 0.21 a 1.01 ± 0.05 a 0.11 ± 0.01 B
TrAFS 5.60 ± 0.04 b 6.00 ± 1.79 ab 21.00 ± 1.79 c 1.86 ± 0.22 b 0.60 ± 0.05 b 0.18 ± 0.04 Ab
RegFor 5.16 ± 0.10 c 2.00 ± 0.55 b 19.20 ± 0.49 c 1.64 ± 0.27 b 0.58 ± 0.07 b 0.44 ± 0.13 A
10–20 cm
OPlow 6.00 ± 0.10 a 15.00 ± 6.39 a 104.67 ± 12.31 a 3.04 ± 0.32 a 0.95 ± 0.07 a 0.13 ± 0.03 B
OPhigh 5.61 ± 0.11 b 7.07 ± 2.82 ab 44.60 ± 9.67 b 2.59 ± 0.24 a 0.81 ± 0.05 a 0.18 ± 0.03 B
TrAFS 5.34 ± 0.04 bc 4.00 ± 1.05 bc 19.20 ± 0.49 b 1.42 ± 0.16 b 0.46 ± 0.04 b 0.34 ± 0.07 Ab
RegFor 5.16 ± 0.07 c 1.20 ± 0.20 c 18.80 ± 0.97 b 1.40 ± 0.18 b 0.50 ± 0.06 b 0.44 ± 0.10 A
20–30 cm
OPlow 5.72 ± 0.14 a 3.67 ± 1.78 a 67.13 ± 12.44 a 1.82 ± 0.23 a 0.83 ± 0.22 a 0.22 ± 0.07 A
OPhigh 5.23 ± 0.15 ab 2.13 ± 0.34 a 34.33 ± 8.53 b 1.50 ± 0.24 a 0.53 ± 0.02 a 0.41 ± 0.09 A
TrAFS 5.28 ± 0.07 a 3.40 ± 0.68 a 17.20 ± 0.80 b 1.20 ± 0.17 a 0.48 ± 0.05 a 0.48 ± 0.11 A
RegFor 5.10 ± 0.14 b 1.00 ± 0.00 a 19.40 ± 5.67 b 1.08 ± 0.23 a 0.46 ± 0.05 a 0.58 ± 0.14 A
30–50 cm
OPlow 5.39 ± 0.13 a 2.13 ± 1.0 a 41.27 ± 8.41 a 1.26 ± 0.19 a 0.50 ± 0.05 a 0.39 ± 0.13 A
OPhigh 5.05 ± 0.14 a 1.53 ± 0.2 a 27.73 ± 6.16 ab 1.09 ± 0.20 a 0.49 ± 0.04 a 0.66 ± 0.15 A
TrAFS 5.22 ± 0.09 a 2.60 ± 0.6 a 16.00 ± 1.10 b 0.98 ± 0.18 a 0.44 ± 0.06 a 0.64 ± 0.11 A
RegFor 5.08 ± 0.10 a 1.00 ± 0.0 a 12.00 ± 0.55 b 0.96 ± 0.25 a 0.42 ± 0.05 a 0.72 ± 0.16 A
Data are the mean ± standard error (n = 5)

sampling locations on the soil carbon stocks. The Results

effect of the oil palm systems on the soil carbon stocks
relative to the agroforestry system (TrAFS) and
regrowth forest (RegFor) was tested using a one-way
analysis of variance. Both analyses were performed
separately for each soil layer. To meet the assumptions
of parametric analysis, data were transformed (natural
logarithm or square root) when required; however,
non-transformed data are presented in the tables and
figures. The Tukey’s test was applied at a 5 %
probability to test the treatment means. The analyses
were performed using SigmaStat version 3.5 (Systat
Software, San Jose, CA, 2008).
The effects of the treatments on soil pH
and nutrients
The oil palm-based agroforestry systems (OPlow and
OPhigh) showed significantly higher soil pH levels and
nutrient (P, K, Ca, and Mg) concentrations as well as
lower soil Al concentrations than the regrowth forest
(RegFor) treatment at the 0–5, 5–10, and 10–20 cm
depths; however, the K concentrations did not differ
between OPhigh and RegFor at a depth of 10–20 cm
(Table 2). At the 0–5, 5–10, and 10–20 cm depths, the

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A B
Fig. 2 Soil carbon concentration (a) and bulk density (b) in
agroforestry systems and regrowth forest in the eastern Amazon
region. Means followed by the same letter in each layer did not
differ based on the Tukey’s test at 5 % probability. Bars
TrAFS treatment showed intermediary values for pH,
nutrients, and Al relative to the results from the
RegFor and oil palm treatments, although most values
were not significantly different from the RegFor
treatment except for the pH (0–5 and 10–20 cm) and
P values (0–5 cm).
At the 20–30 cm depth, only the pH levels and K
concentrations differed significantly among the treat-
ments (Table 2). The RegFor treatment showed the
lowest pH value, although this was not significantly
different from the measured pH of the OPhigh site. The
OPlow treatment had significantly higher K concentra-
tions than did the other treatments.
At the 30–50 cm depth, only the K concentration
varied significantly among the treatments, with higher
values determined for the OPlow site relative to the
TrAFS and RegFor sites. No significant differences
were observed between the oil palm-based AFSs
(Table 2).
The effects of the treatments on the soil C
concentration and bulk density
The soil C concentration differed significantly among
the treatments in all layers except 30–50 cm (Fig. 2a).
In general, the soil C concentrations were lower for the
TrAFS and RegFor treatments than in the oil palm
systems, although the observed differences were not
significant in all layers (Fig. 2a). The oil palm systems
363
represent the standard error. OPlow low species diversity oil
palm-based agroforestry system, OPhigh high species diversity oil
palm-based agroforestry system, TrAFS local traditional agro-
forestry system, and RegFor regrowth forest
differed significantly from each other only at the
10–20 cm depth, with significantly higher soil C
concentrations observed in the OPlow site than in the
OPhigh site (Fig. 2a); the soil C concentrations tended
to be higher for the OPlow site than for the OPhigh site at
depths of 5–10 and 20–30 cm.
The soil bulk density differed significantly among
treatments only at the 0–5, 5–10, and 10–20 cm depths
(Fig. 2b). At these depths, the soil density was
significantly higher at the OPhigh site as compared to
the TrAFS and RegFor sites but did not differ between
the OPhigh and OPlow sites. The soil bulk density for
the OPlow treatment differed significantly from that of
RegFor at 0–5 cm but not from TrAFS; at 5–10 and
10–20 cm, there were no significant differences in the
soil bulk density among the OPlow, RegFor, and
TrAFS sites.
The effects of the treatments on the spatial
variation of soil carbon stocks
The soil C stock was significantly affected by the
treatments (10–20 and 20–30 cm) and by the interac-
tion between the treatments and sampling location
(0–5 cm); no significant effects were observed at 5–10
and 30–50 cm (Table 3). In the 0–5 cm layer of
OPlow, the soil C stock was significantly higher
beneath the canopy and between the oil palm trees
than in the strip. However, for the OPhigh treatment,
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Table 3 Soil carbon stocks at different locations in the oil species) of the oil palm-based agroforestry systems in Tomé-
palm rows (under and between individual oil palm trees) and Açu, eastern Amazon, Brazil
within the strips (composed of herbaceous, shrub, and tree
Soil carbon stock (Mg ha-1)
0–5 cm 5–10 cm 10–20 cm 20–30 cm 30–50 cm

OPlow
Under oil palm 15.3 ± 1.5 aA 12.9 ± 0.5 aA 25.3 ± 0.9 aA 20.3 ± 1.7 aA 32.1 ± 2.1 aA
Between oil palm 15.4 ± 0.7 aA 14.2 ± 1.0 aA 29.4 ± 3.1 aA 19.3 ± 1.3 aA 24.4 ± 0.8 aA
Strip 9.6 ± 1.1 bA 11.6 ± 1.6 aA 25.3 ± 1.0a aA 16.5 ± 1.7a aA 24.1 ± 2.1 aA
OPhigh
Under oil palm 12.7 ± 2.3 aA 11.8 ± 0.6 aA 20.9 ± 1.3 aB 15.3 ± 1.5 aB 25.7 ± 2.5 aA
Between oil palm 10.6 ± 0.5 aA 12.9 ± 0.8 aA 21.0 ± 2.8 aB 14.6 ± 1.7 aB 26.2 ± 2.5 aA
Strip 17.0 ± 1.4 bB 12.1 ± 1.4 aA 23.3 ± 1.9 aB 15.0 ± 0.8 aB 24.5 ± 0.7 aA
For each soil layer, means (±standard error) followed by the same lowercase letter within the sampling position or uppercase letters
between treatments did not differ based on the Tukey’s test at 5 % probability
Data are the mean ± standard error (n = 5)
OPlow low species diversity oil palm-based agroforestry system, OPhigh high species diversity oil palm-based agroforestry system
a
Indicates a significant difference between the overall mean of the sampling positions of the treatments

the soil C stock at 0–5 cm was significantly higher in Discussion

the strip than under the oil palms. At the intermediate
depths (10–20 and 20–30 cm), all of the sampling
locations showed significantly higher soil carbon
stocks for the OPlow site than for the OPhigh site
(Table 3). The soil carbon stock in the strip was
significantly higher for the OPhigh site than for the
OPlow site at 0–5 cm (Table 2).
The effects of the treatments on the soil net carbon
accumulation
The differences in the C stocks among the treatments
generally followed a consistent pattern: the mean C
stocks in the oil palm systems were higher than in the
RegFor and TrAFS treatments at all depths, and there
were significant differences between the surface layers
(0–5, 5–10, and 10–20 cm) except for a lack of
differences among the OPlow, TrAFS, and RegFor sites
at 0–5 cm (Table 4). Considering the entire soil profile
(0–50 cm), the C stocks were also significantly higher
in the oil palm-based AFSs than in the RegFor and
TrAFS sites.
The net soil C accumulation was not significantly
different between the oil palm-based AFSs, which
showed significantly higher values than did the TrAFS
treatment (Fig. 3).
Agroforestry systems alter soil fertility and density
The measured soil nutrient levels, Al concentrations,
and pH values of the regrowth forest site were typical
of low-nutrient acid tropical Oxisols (Sanchez 1976).
To allow for viable crop production in these soils, the
soil fertility must be improved, which is typically
accomplished through liming and fertilization to
increase the soil pH and alleviate P deficiency and
Al toxicity (Vlek et al. 1997). In our study area, the
altered pH, nutrient levels, and Al values can be
attributed to the effects of the soil management of the
oil palm-based treatments: (a) the effects of liming
after land preparation continued to be reflected in the
increased soil pH and Ca and Mg concentrations and
reduced Al concentration; (b) the use of reactive rock
phosphate resulted in higher P concentrations; and
(c) the remarkably high K concentrations were likely
related to the application of K-rich oil palm bunches
(Udotek 2012). Although the same rate of oil palm
bunch application was used in both of the oil palm-
based treatments, the large differences in K concen-
trations that were observed within the 0–30 cm soil
interval may be linked to the differences in plant
diversity between these treatments. The high density

123
Agroforest Syst (2014) 88:357–368 365

Table 4 Soil carbon stocks at different depths in the treatment and OPhigh, respectively), a 9-year-old traditional agroforestry
plots evaluated in 2.5-year-old low species diversity and high system (TrAFS), and a 10-year-old regrowth forest in Tomé-
species diversity oil palm-based agroforestry systems (OPlow Açu (RegFor), eastern Amazon
Soil layer (cm) Soil carbon stock (Mg ha-1)
OPlow OPhigh TrAFS RegFor

0–5 9.9 ± 0.4 ab 12.1 ± 1.0 a 7.5 ± 0.8 b 9.2 ± 0.5 b

5–10 11.9 ± 1.0 a 11.8 ± 0.3 a 7.7 ± 0.7 b 8.9 ± 0.4 b
10–20 24.8 ± 0.9 a 21.3 ± 1.3 a 13.9 ± 1.0 b 14.7 ± 1.0 b
20-30 18.2 ± 1.0 a 16.0 ± 1.0 a 14.6 ± 1.4 a 13.9 ± 1.0 a
30–50 26.9 ± 1.3 a 26.3 ± 0.6 a 24.7 ± 1.9 a 24.2 ± 1.4 a
0–50 91.8 ± 3.1 a 87.6 ± 3.3 a 68.4 ± 4.9 b 71.0 ± 2.4 b
Means (±standard error) followed by the same letters between systems in each soil layer did not differ based on the Tukey’s test at
5 % probability
Data are the mean ± standard error (n = 5)
OPlow low species diversity oil palm-based agroforestry system, OPhigh high species diversity oil palm-based agroforestry system,
TrAFS local traditional agroforestry system, RegFor regrowth forest

resulted in soil compaction for all layers except for the

deepest intervals (20–30 and 30–50 cm). This result is
consistent with the known effects of soil compaction
after deforestation and subsequent mechanized agricul-
tural practices (Hamza and Anderson 2005). Despite the
increased soil bulk density in the oil palm systems, the
maximum average value (1.53 ± 0.02 Mg m-3 at
20–30 cm) in the sandy loam and sandy clay loam
plough layers in our plots was below the threshold of
root growth limitation reported by Reichert et al. (2003),
i.e., 1.40–1.50 Mg m-3 for clay loam and
1.70–1.80 Mg m-3 for sandy loam soils.

Fig. 3 Net soil carbon accumulation (0–50 cm depth) in
agroforestry systems relative to the reference area (regrowth
forest) in the eastern Amazon. OPlow low species diversity oil
palm-based agroforestry system, OPhigh high species diversity
oil palm-based agroforestry system, TrAFS local traditional
agroforestry system
of Musa sp. in the OPhigh plots might have represented
a large aboveground sink for K because this species
has a high demand for this nutrient (Moreira and
Fageria 2009), which resulted in almost two-times less
soil K for this treatment than for the OPlow treatment.
Because Musa sp. was not planted in the OPlow plots,
the demand for K was likely lower, and most of this
nutrient remained in the soil.
The significant differences in the soil bulk density in
the oil palm systems relative to the RegFor and TrAFS
treatments indicated that the mechanized chop-and-
mulch of forest regrowth for oil palm cultivation
Species differences did not have a strong effect
on carbon stocks
Our capacity to infer species effects on carbon stocks
was restricted due to the higher input of (organic)
fertilizers in the OPhigh treatment as compared to the
other treatments. If higher C stocks had been observed
in the OPhigh treatment as predicted, we would not have
been able to differentiate the roles of species diversity
and fertilization rate. In addition, lower carbon stocks
were expected in the OPlow treatment because of the
lower fertilizer inputs. However, we did not find
differences in the carbon stocks between the two oil
palm-based treatments. Our data do not readily explain
this result, although we suggest two possible explana-
tions. First, the occurrence of grasses and kudzu
(Pueraria sp.), which was not measured in our study,
was visibly greater in the OPlow plots than in the OPhigh

123
366
plots, which was likely a result of less shadowing in the
former treatment. It is known that the photosynthesis,
growth and biomass accumulation of grass (C4 plant)
and/or Pueraria is rapid and significant under open,
high light conditions (Forseth and Teramura 1987;
Lambers et al. 2008). Second, the land use history may
not have been homogeneous throughout the entire
experimental area, potentially leading to unseen differ-
ences between the treatments. One formerly common
agricultural practice in the study area was the applica-
tion of organic manure in pits near areas of planted
black pepper (P. nigrum), which may have resulted in
higher-than-expected soil carbon concentrations in the
experimental area, especially for the OPlow area, which
was closest to the road and most likely more intensively
cultivated because of better access.
Short-term changes in soil carbon stocks in oil
palm-based agroforestry systems
In general, the conversion of forests to agricultural
lands leads to a decrease in soil carbon levels (Lal
2005). In this study, however, the conversion of
regrowth forest to oil palm production systems
increased the soil carbon stocks. Mutuo et al. (2005)
stated that the rehabilitation of agricultural land and
pastures with AFSs increased carbon stocks of the
vegetation and soil within several years, as reported
for 25-year experiments in the tropics (Palm et al.
2000; Hairiah et al. 2001). Our results also corroborate
findings of other authors who reported that the
adoption of conservation practices such as zero tillage
increases the soil carbon stocks; these effects are more
apparent in the soil surface layers and are related to the
annual supply of plant residues to the soil (Bayer et al.
2002; Diekow et al. 2005).
The soil carbon stock of the regrowth forest is within
the range of variation reported in similar studies for this
type of vegetation. For example, Bernoux et al. (1998)
found values of 20.4 Mg C ha-1 in the 0-10 cm layer
in 10-year-old regrowth forest in the eastern Amazon.
Relatively high values are not uncommon, such as those
reported by Silva et al. (2009) for the 0–10 cm layer in
regrowth forest in a clayey Oxisol (34.5 Mg C ha-1).
In addition to the influence of soil texture, the variation
in soil carbon stocks in regrowth forests depends largely
on the land-use history, which affects biomass accu-
mulation (Zarin et al. 2005) and, consequently, carbon
inputs to soil.
123
Agroforest Syst (2014) 88:357–368
Our results suggest that within the studied region,
traditional AFSs, which are usually subject to burning
during land preparation and are planted with species
such as T. cacao, E. oleracea, and P. nigrum, have a
limited capacity for mitigating the effects of climate
change. However, older AFSs and/or those with
different species compositions may be able to restore
soil carbon stocks. For example, the soil carbon stock
down to a depth of 50 cm in 9- and 14-year-old AFSs
(mean = 85.2 ± 4.1 Mg ha-1) with different planted
species compositions did not differ significantly from
the C stocks in an approximately 30-year-old regrowth
forest (mean = 97.9 ± 2.3 Mg ha-1) in Tomé-Açu
(Brancher 2010).
The oil palm-based AFSs showed a high extent of
soil carbon accumulation, suggesting that these sys-
tems were efficient in storing the carbon available
from reduced biomass loss associated with fire-free
land preparation as well as increased carbon inputs
through organic fertilization. It is important to note
that the improved soil fertility in the oil palm-based
AFSs may also have played a role in the soil carbon
accumulation in these systems. In Costa Rica, larger
soil C pools in conventional coffee agroforests com-
pared to organic coffee agroforests have been associ-
ated with a positive interaction between mineral
fertilizer and C inputs in the conventional coffee
agroforests (Tully et al. 2013).
Despite early soil C stock increases in the oil palm-
based treatments, the labile component must be
differentiated from the recalcitrant soil C pool (Janzen
et al. 1992; Duxbury et al. 1989) because this
distinction may be very important for determining
the potential of each oil palm-based agroforestry
system to mitigate climate change. Further research on
soil organic matter fractionation in the oil palm-based
AFSs is warranted.
Spatial variation of the soil carbon stocks in the oil
palm systems
In general, no clear effect of oil palm systems on soil C
stock spatial variation could be identified, which may
be related to the young age of the systems. In
conventional oil palm systems, spatial variation in the
soil C has been demonstrated for plantations older than
those in our study (Frazão et al. 2012; Law et al. 2009).
However our results suggest that management practices
affected the spatial variation of soil C stocks in our
Agroforest Syst (2014) 88:357–368
study. In addition to the high amount of fasciculate
(fine) surface roots that are common to oil palm trees
(Jourdan and Rey 1997), the sidedressing nutrient
application may have represented an important source
of surface carbon input. Prior to our soil sampling,
approximately 82 Mg ha-1 of organic fertilizer was
applied in the strip area, which is consistent with the
higher soil C stock found in the strip than beneath the
crown or between oil palm trees for the OPhigh
treatment. It is likely that inputs from litterfall (Chander
et al. 1998) and sidedressing of the tree species (30 kg
of organic fertilizer per plant) further increased the soil
C stock in the strips of the OPhigh treatment. Conse-
quently, the lower carbon stock in the strip portion of
the OPlow area may be related to the lower inputs of
organic fertilizer (*26 Mg ha-1) and litterfall (data
not available) compared to the strips in the OPhigh area.
Conclusions
Conversion from regrowth forest to an oil palm-based
AFSs did not negatively impact soil carbon stocks. The
early net accumulation of soil C in the young (2.5-year-
old) oil palm-based AFS was high, likely reflecting the
combination of fire-free land preparation, organic
fertilization, and the input of plant residues from
pruning and weeding. A strong spatial variability in the
soil C stocks was not detected, which was most likely
attributed to the young age of our oil palm-based AFSs;
however, organic fertilization management appears to
have an important role in influencing the differences in
soil C stocks between the oil palm and strip areas.
Acknowledgments We are indebted to Mr. Ernesto Suzuki for
granting permission to use the experimental area. This project
was funded by Natura Inovacao e Tecnologia de Produtos Ltda.,
Cooperativa Mista de Tome-Açu(CAMTA), Ministerio da
Ciencia e Tecnologia (MCT), and the Empresa Brasileira de
Pesquisa Agropecuaria (EMBRAPA). We wish to thank the
team of the Laboratorio de Ecofisiologia Vegetal of Embrapa
Amazonia Oriental. We also thank two anonymous reviewers
for their insightful comments that improved the manuscript.
References
Baena ARC, Falesi IC (1999) Avaliação do potencial quı́mico e
fı́sico dos solos sob diversos sistemas de uso da terra na
Colônia Agrı́cola de Tomé-Açu, Estado do Pará. Boletim
de Pesquisa, 18. Embrapa Amazônia Oriental, Belém, p 23
367
Bayer C, Dick DP, Ribeiro GM, Scheuermann KK (2002)
Carbon stocks in organic matter fractions as affected by
land use and soil management, with emphasis on no-tillage
effect. Cienc Rural 32:401–406
Bernoux M, Cerri CC, Neill C, Moraes JL (1998) The use of
stable carbon isotopes for estimating soil organic matter
turnover rates. Geoderma 82:43–58
Brady NC (1996) Alternatives to slash-and-burn: a global
imperative. Agric Ecosys Environ 58:3–11
Brancher T (2010) Estoque e ciclagem de carbono de sistemas
agroflorestais em Tomé-Açu, Amazônia Oriental. Thesis,
Universidade Federal do Pará, Belém
Brasil (2011) Programa nacional de produção e uso do biodiesel.
http://www.biodiesel.gov.br/. Accessed 5 Apr 2011
Chander K, Goyal S, Nandal DP, Kapoor KK (1998) Soil
organic matter, microbial biomass and enzyme activities in
a tropical agroforestry system. Biol Fertil Soils 27:168–172
Davidson EA, Sá TDDA, Carvalho CJR, Figueiredo RDO, Kato
MDSA, Kato OR, Ishida FY (2008) An integrated green-
house gas assessment of an alternative to slash-and-burn
agriculture in eastern Amazonia. Glob Change Biol
14:1–10
Denich M, Vielhauer K, Kato M, Block A, Kato OR, Sá T,
Lücke W, Vlek PLG (2004) Mechanized land preparation
in forest-based fallow systems: the experience from East-
ern Amazonia. Agrofor Syst 61–62(1–3):91–106
Desjardins T, Barros E, Sarrazin M, Girardin C, Mariotti A
(2004) Effects of forest conversion to pasture on soil car-
bon content and dynamics in Brazilian Amazonia. Agric
Ecosyst Environ 103(2):365–373
Diekow J, Mielniczuk J, Knicker H, Bayer C, Dick DP, Kögel-
Knabner I (2005) Soil C and N stocks as affected by
cropping systems and nitrogen fertilization in a southern
Brazil Acrisol managed under no-tillage for 17 year. Soil
Tillage Res 81:87–95
Duxbury JM, Smith MS, Doran JW (1989) Soil organic matter
as a source and sink of plant nutrients. In: Coleman DC,
Oades JM, Uehara G (eds) Dynamics of soil organic matter
in tropical ecosystems. University of Hawaii, Honolulu,
pp 33–67
Embrapa (1997) Manual de metodos de analise de solo, 2nd edn.
EMBRAPA-CNPS, Rio de Janeiro
Forseth IN, Teramura AH (1987) Field photosynthesis, micro-
climate and water relations of an exotic temperate liana,
Pueraria lobata, kudzu. Oecologia 71:262–267
Frazão LA, Paustian K, Pellegrino Cerri CE, Cerri CC (2012)
Soil carbon stocks and changes after oil palm introduction
in the Brazilian Amazon. GCB Bioenergy. doi:10.1111/j.
1757-1707.2012.01196.x
Häger A (2012) The effects of management and plant diversity
on carbon storage in coffee agroforestry systems in Costa
Rica. Agrofor Syst. doi:10.1007/s10457-012-9545-1
Hairiah K, Sitompul SM, van Noordwijk M, Palm CA (2001)
Carbon stocks of tropical land use systems as part of the
global carbon balance: effects of forest conversion and
options for clean development activities. Alternatives to
slash-and-burn (ASB) Lecture Note 4. ICRAF, Bogor,
Indonesia
Hamza MA, Anderson WK (2005) Soil compaction in cropping
systems: a review of the nature, causes and possible solu-
tions. Soil Tillage Res 82:121–145
123
368
Janzen HH, Campbell CA, Brandt SA, Lafond GP, Townley-
Smith L (1992) Light-fraction organic matter in soils from
long-term crop rotations. Soil Sci Soc Am J 56:1799–1806
Jourdan C, Rey H (1997) Architecture and development of the
oil-palm (Elaeis guineensis Jacq.) root system. Plant Soil
189:33–48
Lal R (2005) Soil carbon sequestration in natural and managed
tropical forest ecosystems. J Sustain For 21:1–30
Lambers H, Chapin FS III, Pons TL (2008) Plant physiological
ecology. Springer, New York
Law MC, Balasundram SK, Ahmed OH, Harun MH (2009)
Spatial variability of soil organic carbon in oil palm. Int J
Soil Sci 4:93–103
Moreira A, Fageria NK (2009) Yield, uptake, and retransloca-
tion of nutrients in banana plants cultivated in upland soil
of Central Amazonian. J Plant Nutr 32:443–457. doi:10.
1080/01904160802660750
Mutuo PK, Cadisch G, Albrecht A, Palm CA, Verchot L (2005)
Potential of agroforestry for carbon sequestration and
mitigation of greenhouse gas emissions from soils in the
tropics. Nutr Cycl Agroecosyst 71:43–54
Neumann-Cosel L, Zimmermann B, Hall JS, van Breugel M,
Elsenbeer H (2011) Soil carbon dynamics under young
tropical secondary forests on former pastures—a case study
from Panama. For Ecol Manag 261(10):1625–1633.
doi:10.1016/j.foreco.2010.07.023
Palm CA, Woomer PL, Alegre J, Arevalo L, Castilla C, Cordeiro
DG, Feigl B, Hairiah K, Kotto-Same J, Mendes A, Mou-
kam A, Murdiyarso D, Njomgang R, Parton WJ, Ricse A,
Rodrigues V, Sitompul SM, van Noordwijk M (2000)
Carbon sequestration and trace gas emissions in slash-and-
burn and alternative land uses in the humid tropics.
Alternatives to Slash-and-Burn Programme, Nairobi
Reichert JM, Reinert DJ, Brada JA (2003) Qualidade dos solos e
sustentabilidade de sistemas agrı́colas. Ci Ambiente
27:29–48
Sanchez PA (1976) Properties and management of soils in the
tropics. Wiley, New York
123
Agroforest Syst (2014) 88:357–368
Silva M Jr, Desjardins T, Sarrazin M, Melo V, Martins P, Santos
ER, Carvalho C (2009) Carbon content in Amazonian
Oxisols after forest conversion to pasture. Rev Bras Cienc
Solo 33:1603–1611
Sisti CPJ, Santos H, Kohhann R, Alves BJR, Urquiaga S,
Boddey RM (2004) Change in carbon and nitrogen stocks
in soil under 13 years of conventional or zero tillage in
southern Brazil. Soil Tillage Res 76:39–58
Smith NJH, Fik TJ, PdT A, Falesi IC, Serrão EAS (1995)
Agroforestry developments and potential in the Brazilian
Amazon. Land Degrad Dev 6(4):251–263. doi:10.1002/ldr.
3400060406
Sommer R, Vlek PLG, Sá T, Vielhauer K, Coelho R, Fölster H
(2004) Nutrient balance of shifting cultivation by burning
or mulching in the Eastern Amazon—evidence for subsoil
nutrient accumulation. Nutr Cycl Agroecosyst 68:257–271
Tully KL, Lawrence D, Wood SA (2013) Organically managed
coffee agroforests have larger soil phosphorus but smaller
soil nitrogen pools than conventionally managed agrofor-
ests. Biogeochemistry 115:385–397. doi:10.1007/s10533-
013-9842-4
Udotek IA (2012) Characterization of ash made from oil palm
empty fruit bunches. Int J Environ Sci 3:518–524
United States Department of Agriculture—USDA (2012) Pro-
duction, supply and distribution. http://www.fas.usda.gov/
psdonline/psdQuery.aspx. Accessed 2 Mar 2012
Vlek PLG, Kühne RF, Denich M (1997) Nutrient resources for
crop production in the tropics. Phil Trans R Soc Lond B
352:975–985
Yui S, Yeh S (2013) Land use change emissions from oil palm
expansion in Pará, Brazil depend on proper policy
enforcement on deforested lands. Environ Res Lett 8:1–9
Zarin DJ, Davidson EA, Brondizio E, Vieira ICG, Sá T,
Feldpausch T, Schuur EAG, Mesquita R, Moran E, Dela-
monica P, Ducey MJ, Hurtt GC, Salimon C, Denich M
(2005) Legacy of fire slows carbon accumulation in
Amazonian forest regrowth. Frontiers Ecol Environ
3(7):365–369