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Carbon neutral expansion of oil palm plantations
in the Neotropics
Juan Carlos Quezada
1,2
*, Andres Etter
3
, Jaboury Ghazoul
4,5,6
,
Alexandre Buttler
1,2,7
, Thomas Guillaume
1,2
Alternatives to ecologically devastating deforestation land use change trajectories areneeded to reduce the carbon
footprint of oil palm (OP) plantations in the tropics. Although various land use change options have been proposed,
so far, there are no empirical data on their long-term ecosystem carbon pools effects. Our results demonstrate that
pasture-to-OP conversion insavanna regions does not changeecosystem carbon storage, after 56 years in Colombia.
Compared to rainforest conversion, this alternative land use change reduces net ecosystem carbon losses by 99.7 ±
9.6%. Soil organic carbon (SOC) decreased until 36 years after conversion, due to a fast decomposition of pasture-
derived carbon, counterbalancing the carbon gains in OP biomass. The recovery of topsoil carbon content, suggests
that SOC stocks mightpartly recover during a third plantation cycle. Hence, greater OP sustainability can be achieved
if its expansion is oriented toward pasture land.
INTRODUCTION
Rainforests have been a major source of land for newly established
oil palm (OP) plantations, particularly in the main OP–producing
countries such as Indonesia and Malaysia (1,2). Conversion of
rainforests to OP plantations negatively affects a number of eco-
system functions including ecosystem carbon (C) storage, soil fer-
tility, and biodiversity (3,4). In Southeast Asia, a global hot spot of
greenhouse gas emission from deforestation and land use change,
deforestation for OP cultivation was the second largest source of
CO
2
emission [~0.3 giga tons (GT) of CO
2
year
−1
](5). Replacement
of forested areas by OP plantations reduces ecosystem C storage
by up to 173 Mg C ha
−1
, owing mainly to the abrupt loss of biomass
(6,7). Such ecosystem C losses are exacerbated when OP plantations
are established on tropical peatlands, as has occurred in Southeast
Asia (8,9).
In response to the detrimental environmental impacts associated
with deforestation, various deforestation-free land use change tra-
jectories have been proposed for a more sustainable OP expansion,
including the use of marginal lands and conversion of savannas and
pasture areas (10,11). Of these, the use of pasture areas has great
interest given the vast amount of land under pastoral systems and
their low biodiversity and biomass C stocks (3,12,13). This land
use change even has potential for climate change mitigation benefits
by increasing C sequestration, given the substantially higher above-
ground biomass C of OP over pastures (11). Yet, large uncertainties
remain (2,14), particularly with respect to changes in total ecosystem
C (TEC) changes, soil organic carbon (SOC) stocks, and other soil
properties. Meta-analysis studies on the conversion of pastures into
perennial plantations (often called afforestation) showed contrasting
SOC stock changes (15,16). Only two recent studies have quantified
the effects of grasslands and pasture conversion into OP planta-
tions on SOC storage, but their results are in disagreement (17,18).
Studies are much more numerous in the typical deforestation land
use change trajectory of OP development on forested land. Most re-
port that forest-to-OP conversion leads to soil degradation and C
losses due to decreased organic matter (OM) inputs and erosion
(4,17,19,20), although a few have noted positive or unclear effects
on SOC (17,21,22). In addition and despite the generally accepted
view on SOC losses in OP plantations and the major role of soil
organic matter (SOM) on soil productivity, soil chemical fertility
and plant nutrient availability appear not to be negatively affected
by OP agriculture, likely due to the use of mineral fertilizers in plan-
tations (4,23).
The reported changes in SOC following land use change to OP
have occurred mainly in the surface layers (0 to 30 cm), and no effects
in the subsoil have been detected. Yet, the focus of the literature to date
has been the first OP rotation cycle (25 to 30 years) or even shorter
time periods, which might not be a sufficient time to realize the effects
of ongoing belowground processes. Evidence from other land use
change types has already demonstrated that time after vegetation
change (16,24,25)andsamplingdepth(26) have major roles on
the magnitude and direction of changes in SOC stocks. The time
following land use change needed for soils to reach either a new C
equilibrium state or a subsequent recovery after the initial C losses
usually occurs only after several decades (25,26). In a recent compre-
hensive review on ecosystem functions in OP, the need to consider
longer-term studies to assess the effects of OP cultivation on eco-
system functions was emphasized (4). The lack of observed responses
in subsoil layers might be explained by the short time periods
considered after land use conversion. Inputs of fresh OM from deep
palm roots and nutrients from leaching might occur and stimulate
the microbial mineralization of the large SOC stocks stored in sub-
soils (27,28). The absence of change in SOC stocks in subsoils does
not necessarily indicate that the old SOC stabilized during the pre-
vious land uses was not affected by the conversion, as it might in-
stead be substituted by new SOC derived from OP inputs. This can
be investigated when OP, which has a C3 photosynthetic pathway, is
1
École Polytechnique Fédérale de Lausanne EPFL, School of Architecture, Civil and
Environmental Engineering ENAC, Laboratory of Ecological Systems ECOS, 1015
Lausanne, Switzerland.
2
Swiss Federal Institute for Forest, Snow and Landscape
Research WSL, Site Lausanne, 1015 Lausanne, Switzerland.
3
Department of Ecol-
ogy and Territory, Pontificia Universidad Javeriana, Bogota, Colombia.
4
Chair of
Ecosystem Management, Institute of Terrestrial Ecosystems, Department of
Environmental Systems Science, ETHZ, 8092 Zürich, Switzerland.
5
Prince Bernhard
Chair for International Nature Conservation, Ecology and Biodiversity, Utrecht Uni-
versity, Padualaan 8, 3584 CH, Utrecht, Netherlands.
6
Centre for Sustainable
Forests and Landscapes, University of Edinburgh, King’s Buildings, Alexander Crum
Brown Road, Edinburgh EH9 3FF, Scotland.
7
Laboratoire de Chrono-Environnement,
UMR CNRS 6249, UFR des Sciences et Techniques, 16 route de Gray, Université de
Franche-Comté, 25030 Besançon, France.
*Corresponding author. Email: quezadarivera@gmail.com
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established on tropical pastures or savannas, which are dominated by
grasses having a C4 photosynthetic pathway (29). The different frac-
tionation intensities of the two photosynthetic pathways result in dif-
ferences in the isotopic signature (d
13
C) of the biomass, enabling the
origin of SOC to be determined (30). This provides a powerful tool to
study decomposition and stabilization of SOC after land use change.
In Colombia, the expansion of OP plantations has occurred mainly
on pastures planted on cleared savannas and, to some extent, also
on native tropical savannas. These land use changes contrast with the
deforestation trajectories of the main OP–producing countries in
Southeast Asia (14,31). OP coverage in Colombia, which is currently
the fourth major OP producer worldwide, has increased rapidly,
tripling in the last two decades from roughly 160,000 to 480,000 ha
(32). Of this expansion, about 60% involved the use of low productivity
pasture areas (31). Nearly half of the land devoted to OP cultivation
in Colombia occurs in the Llanos region of eastern Colombia, where
cattle ranching is the main land use (33,34), and future scenarios
predict a fast growth rate of the OP industry in this region (31).
This study aims to assess the pasture-to-OP transition as an alter-
native to deforestation to mitigate the net TEC losses of future OP ex-
pansion. Specifically, we hypothesized that C gains in OP biomass
might be counterbalanced by C losses in the soil. SOC stocks would
be affected down to 50 cm, but a new equilibrium would be reached
in all layers after two rotation cycles. Because of the long-term chemical
fertilization in OP plantations, we expect to observe trade-offs among
soil ecosystem services such as C storage and nutrient provision. To test
these hypotheses, we quantified the dynamics of OP biomass C stocks,
OP-, and pasture-derived SOC stocks down to 50 cm and nutrient avail-
ability over a long-term 56-year chronosequence of OP plantations
established on former pastures in Colombia, taking advantage of a shift
from C4 to C3 vegetation.
RESULTS
Soil C stock dynamics
Cultivation of OP on former pasture areas severely affected SOC
stocks to a depth of 50 cm (Fig. 1). Of the 102 ± 8 Mg C ha
−1
stored
in pasture SOC 39 ± 8% were lost after 56 years of OP cultivation.
However, the C loss dynamics followed neither a linear nor an
exponential trend but, rather, two trends in one adjusting to a seg-
mented regression model (Fig. 1 and table S1). SOC stocks down to
50 cm constantly decreased until the beginning of the second OP
cycle (break point, 36.1 ± 9.0 years) at a rate of 1.26 ± 0.26 Mg C
ha
−1
year
−1
, after which SOC stocks stabilized along the second OP
rotation cycle.
The dynamics of the total SOC stocks down to 50 cm resulted
from the combination of variable rates and patterns in the accumu-
lation of OP-derived C and decomposition of pasture-derived C at
different depths (Fig. 2). In the surface soil layer (0 to 10 cm), bulk
SOC stocks decreased sharply at a rate of 0.42 ± 0.08 Mg C ha
−1
year
−1
until 39.1 ± 4.5 years and then stabilized for the rest of the cultiva-
tion time. The initial decline in bulk SOC stocks was driven by a
marked loss of pasture-derived C (77% after 39 years) that was
not fully compensated by the accumulation of OP-derived C during
thesameperiodoftime(Fig.2A).Thedecompositionofpasture-
derived SOC followed a first-order decay with a half-life time of
18.7 years (k= 0.037 ± 0.0038; Table 1). The accumulation of OP-
derived SOC in the surface soil layer was best fitted by an exponential
rise to equilibrium model, indicating a saturation in the accumulation
of OP-derived C. The estimated gross OP-derived C input was of
0.62 ± 0.10 Mg C ha
−1
year
−1
, and its annual decay rate was of 0.038 ±
0.010 year
−1
. The decay rate constants of SOM between OP-derived
and pasture-derived C were similar, suggesting no preferential C
source for decomposers.
Fig. 1. Soil carbon stocks after pasture conversion into OP plantations at 0- to 50cm depth. The dashed line represents the fitted segmented regression equation.
Significance of the slope coefficients from each side of the breaking point is indicated (***P< 0.001).
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At break point (39 years), the net difference between the kinetic
rates of change (according to the differencebetween the first derivative
of Eqs. 4 and 5) was very low (−0.13 Mg C ha
−1
year
−1
). SOC stocks in
the top 10 cm would reach equilibrium at 16.33 Mg ha
−1
(calculated as
division between Aand kparameters of Eq. 4), accordingto the model
based on C isotopes, i.e., similar level to the one estimated by the seg-
mented regression based on bulk SOC (15.46 Mg C ha
−1
; Table 1).
These lattertwo estimations cross-validated the two approaches (bulk
SOC and isotopic) used to estimate C dynamic in this work.
The SOC bulk stock dynamics in the two deeper soil layers (10- to
20-cm and 20- to 30-cm) exhibited similar patterns, i.e., a constant
decrease followed by a stabilization of the stocks along the second
rotation (Fig. 2, B and C, and Table 1). However, the C loss rates
for these two soil layers were 14 and 46% less pronounced than those
for the surface soil layer but stabilized at similar time: 37.8 ± 4.4 and
38.9 ± 10.3 years for the 10- to 20-cm and 20- to 30-cm soil depths,
respectively. The decomposition of pasture-derived SOC also followed
an exponential decay in the 10- to 20-cm and 20- to 30-cm layers. The
decay rates, however, were lower, resulting in longer half-life of these
pools, as compared to the surface layer (18.7, 34.7, and 40.8 years for
the 0- to 10-cm, 10- to 20-cm, and 20- to 30-cm soil depths, respective-
ly). In contrast to surface soil layer, the accumulation of OP-derived C
did not show any saturation, with constant accumulation rates of
0.10 ± 0.01 and 0.07 ± 0.01 Mg C ha
−1
year
−1
for the 10- to 20-cm
and 20- to 30-cm layers, respectively, throughout the two rotation cycles
(Fig. 2, B to D, and Table 1).
As indicated above, bulk SOC stocks reached an equilibrium in
the 0- to 30-cm layer. In contrast, bulk SOC stocks in the deepest
soil layer (30 to 50 cm) were still decreasing at a rate of 0.25 Mg C
ha
−1
year
−1
±0.04(R
2
= 0.71; Table 1) after 56 years. This finding is of
interest as no studies have reported, so far, effects of land use change
to OP in subsoil horizons. The obtained C loss rates for bulk SOC
stocks (slope 1 for three uppermost soil layers and linear regression
slope for the deepest layer) decreased gradually with soil depth from
0.42 Mg C ha
−1
year
−1
in the surface of 10 cm to 0.13 Mg C ha
−1
year
−1
in the 30- to 40-cm and 40- to 50-cm soil depth (calculated from half
of the depth of 30 to 50 cm).
Ecosystem C stocks
OP plantations contain substantially greater total biomass (above-
and belowground) than pastures. Total OP biomass increased at an
accumulation rate of 3.3 ± 0.1 Mg C ha
−1
year
−1
along the 30 years
of both, the first and the second OP cultivation cycles. This corre-
sponded to time-averaged OP biomass C stocks of 49.5 ± 1.5 Mg C
ha
−1
, i.e., five times more than 10 Mg C ha
−1
typically found in the
pastures of this region (35,36). Although the SOC stock varied with
plantation age, in general, soil was the largest C pool in the ecosystem.
The contribution of SOC to TEC stocks ranged from 38% in the
30-year-old first cycle plantation to 87% in the recently replanted plan-
tation 2-year-old second cycle plantation (32 years).
Time-averaged TEC in pastures reached 112.8 ± 8.3 Mg C ha
−1
,
assuming constant SOC stocks (102.8 ± 8.3 Mg C ha
−1
) and a total
pasture biomass of 10 Mg C ha
−1
(Fig. 3). Over a large number of
OP rotation cycles, time-averaged SOC stocks in OP plantations
would be equal to the stocks at equilibrium (62.61 ± 2.73 Mg C
ha
−1
; Fig. 1). Accordingly, time-averaged TEC in OP plantations
Fig. 2. Dynamics of pasture C4-derived C and OP C3-derived C following pasture conversion into OP plantations. (A) 0- to 10-cm soil layer, (B) 10- to 20-cm soil
layer, (C) 20- to 30-cm soil layer, and (D) 30- to 50-cm soil layer. Inset graphs show bulk SOC stocks for each layer. See Table 1 for the used functions and their
kinetic parameters.
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reaches 112.3 ± 3.2 Mg C ha
−1
(Fig. 3). This indicates that the con-
version of pastures to OP plantations in this region is close to C
neutrality (−0.5 ± 8.8 Mg C ha
−1
) considering multiple OP cycles.
The rate of C accumulation in the biomass was higher (3.3 ± 0.1 Mg C
ha
−1
year
−1
) than the rate ofSOC losses (1.26 ± 0.3 Mg C ha
−1
year
−1
).
As a result, TEC during the first rotation cycle was always higher than
in pasture, but only about half of the time for the subsequent second
rotation cycle when SOC stocks have reached equilibrium (Fig. 3).
Therefore, OP plantations were continuously a C sink, even during
the phase of SOC losses, except at the time of plantation replanting
when OP biomass is destroyed.
Soil fertility
SOC content, unlike SOC stocks, increased significantly after 41.1 ±
2.7 years following an initial decline in the 0- to 10-cm. However, this
C recovery did not reach the initial soil C content present under pasture
(2.5 ± 0.1%; Fig. 4A). The rate of increase in soil C content was almost
thedoubleascomparedtothedecrease(−0.03 ± 0.02%). This partial
recovery of SOC content was observed down to a depth of 30 cm but
not below where SOC content was still decreasing linearly (R
2
= 0.75)
after 56 years of OP cultivation.
Macronutrient availability was strongly enhanced down to 50-cm
depth (table S2). The sum of cations showed a decreasing trend with
depth at all sites. Nonetheless, all layers exhibited a similar enrich-
ment factor of 3.9 to 5.6 of the sum of cations, indicating nutrient
leaching of the applied nutrients by fertilization. Nutrient enrich-
ment did not show any saturation with time (Fig. 4B). Base satura-
tion (BS) increased in the four layers, up to a factor of four, 56 years
after conversion in the 30- to 50-cm-depth layer. Available Bray P
showed a different pattern. It peaked at 18.0 ± 5.3 years and then
levelled off at higher levels than in pastures in the top 10 cm (Fig. 4C).
This same pattern with small variations in the estimated break point
was found for the 30- to 50-cm soil depth. However, a significant de-
crease during the last years of the first cycle and the entire second
cycle followed the observed peak. This suggests the leaching of Pinto
the subsoilin the short term (first OP cycle). Soil pH valuesexhibited a
narrow range from 4.0 to 4.6 across land uses and soil depths.
OP cultivation did not have a constant effect throughout the two
rotation cycles and soil depth, as shown by principal components
analysis (PCA; Fig. 5). During the first cycle, the amount (SOC con-
tent) and quality (C/N ratio) of OM decreased, while the nutrients
and bulk density (BD) increased in the surface (0- to 10-cm) and sub-
soil (30- to 50-cm) layers, as shown by the first principal component
Fig. 3. TEC stocks. TEC in OP plantations and pastures includes above- and
belowground biomass and SOC stocks down to 50 cm (but not dead trees after
replanted). The orange diamond and its vertical SE bars correspond to the time-
averaged TEC stocks in pastures. Purple circle and its vertical SE bars correspond
to time-averaged TEC stocks in OP, and purple band indicates the time-averaged
TEC stocks during the 56 years of OP cultivation.
Table 1. List of functions and kinetic parameters. Parameters describe changes in bulk SOC stocks and C3- and C4-derived C stocks in the four sampled soil
layers. R
2
, coefficient of determination; slopes 1 and 2, significance of the two slopes for segmented regression analysis; K, rate constant; A, annual input of C3-C;
C
0
, SOC stocks before pasture change to OP. **P< 0.01; ***P< 0.001.
Soil layer Model type Function R
2
Slope 1 Slope 2 AIC k(year
−1
) Half-life AC
0
Bulk soil, 0- to 10-cm Segmented F(t) = 31.87 −0.42*t0.75 *** NS 88.26 ————
OP-derived C, 0- to 10-cm Exponential rise to equilibrium F(t)=−0.62*exp(−0.038*t) + 0.62/0.038 0.91 ——66.0 ** 18.1 *** —
Pasture-derived C, 0- to 10-cm Single exponential decay F(t) = 31.4*exp(t*−0.037) 0.91 ——86.2 *** 18.7 —***
Bulk soil, 10- to 20-cm Segmented F(t) = 24.49 −0.36*t0.83 *** NS 75.52 ————
OP-derived C, 10- to 20-cm Linear F(t)=−0.27 + 0.10*t0.85 ——46.4 ————
Pasture-derived C, 10- to 20-cm Single exponential decay F(t) = 24.1*exp(t*−0.02) 0.84 ——80.7 *** 34.7 —***
Bulk soil, 20- to 30-cm Segmented F(t) = 19.91 −0.23*t0.75 *** NS 75.08 ————
OP-derived C, 20- to 30-cm Linear F(t)=−0.20 + 0.07*t0.7 ——45.56 ————
Pasture-derived C, 20- to 30-cm Single exponential decay F(t) = 19.8*exp(t*−0.02) 0.79 ——77.7 *** 40.8 —***
Bulk soil, 30- to 50-cm Linear F(t) = 29.42 −0.25*t0.71 ——87.73 ————
OP-derived C, 30- to 50-cm Linear F(t) = 0.02 + 0.10*t0.60 ——66.39 ————
Pasture-derived C, 30- to 50-cm Single exponential decay F(t) = 29.8*exp(t*−0.016) 0.69 ——99 *** 43.3 —***
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(PC1, 35.7% at 0- to 10-cm and 45.1% at 30- to 50-cm). During the
second cycle, the effects of cultivation remained similar in the subsoil
(Fig. 5B), while the surface soil layer showed a partial recovery of SOC
content but not SOC quality, suggesting a slight improvement of top-
soil fertility in the oldest plantations.
DISCUSSION
We demonstrate that the conversion of pasture-to-OP in Colombia
compares favorably in terms of ecosystem C changes to that of
OP expansion into forested lands, as often occurs in major OP–
producing countries in Southeast Asia. While the conversion of rain-
forests in Sumatra (6) led to a loss of 173 Mg C ha
−1
, the conversion
of pasture-to-OP plantation was C neutral (−0.5 ± 8.8 Mg C ha
−1
),
reducing TEC losses by 99.7 ± 9.6%. In addition, establishing OP on
pastures not only avoids the large initial loss of C stored in rainforest
biomass but also increases biomass C pools. Nonetheless, converting
pastures to OP did not act as C sink because the conversion caused
large SOC reductions that counterbalanced the gains in OP biomass C.
The time-averaged C stored in OP biomass is mainly influenced
by the length of rotation cycles (6). Shortening the rotation time to
25 years, as common in Southeast Asia, would reduce the time-
averaged biomass C by 17% (about 8 Mg C ha
−1
), leading to a small
C loss following land use change. OP biomass C found in Colombian
plantations was similar to those reported for Indonesian’s(6,37).
Carbon pools that were not measured in this study, such as frond
piles or understory vegetation if present (<3 Mg C ha
−1
), have a neg-
ligible contribution to TEC (37). The main factor determining whether
Fig. 4. Soil chemical fertility dynamics. (A) Soil C content as a function of time
after pasture conversion into OP plantations at the soil surface (0- to 10-cm). The
yellow line represents the fitted segmented regression equation. Significance
of the slope coefficients from each side of the breaking point is indicated
(***P< 0.001). (B) Sum of cations as a function of time after pasture conversion
into OP plantations at two soil depths: close circles, 0- to 10-cm; open circles,
30- to 50-cm. The lines represent the linear regression equations. (C) Available
phosphorus (Bray P) as a function of time after pasture conversion into OP
plantations at the soil surface (0- to 10-cm). The red line represents the fitted
segmented regression equation. Significance of the slope coefficients from
each side of the breaking point is indicated (***P< 0.001).
Fig. 5. PCA of soil properties in pastures and OP plantations derived from
pastures. (A) The soil surface (0- to 10-cm) and (B) the subsoil (30- to 50-cm). BD,
bulk density; C:N, C and N ratio;
13
C, d
13
C; N, nitrogen; EA, exchangeable acidity;
Na, sodium; K, potassium; Mg, magnesium;
15
N, d
15
N; Ca, calcium; BS, base satu-
ration and P, available phosphorus (Bray P). The OP plots are indicated with time
after conversion in years (yrs).
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the land use change will result in small C gains or losses is the initial
amount of SOC in the converted grassland ecosystem. SOC losses after
land use change are not constant but rather proportional to the initial
SOC stocks (20). The initial variability of SOC stocks in the studied
pastures (SD of 14.3 Mg C ha
−1
) surpassed alone the C stored in grass
biomass. The managed pastures investigated in this study could represent
the land use type with the highest initial SOC storage on well-drained
soils in this region, as Brachiaria pastures favor soil C sequestration
when they replace either forested or grassland areas in the Neotropics
(38,39). In addition, because the rainfall and rainy season length are
higher, soils in the piedmont often harbor slightly higher C stocks than
the savannas further to the east. Lower SOC losses, and thus a slightly
positive change in ecosystem C storage, are therefore expected when
OP plantations are established on degraded pastures or other part of
the Llanos (40). The same argument is often used to justify the trans-
formation of the native savannas, without due regard to the biodiversity
and ecosystem service values of these natural ecosystems. Given that
the Llanos is expected to remain an important OP expansion area
in Colombia, special attention needs to be given to the loss of native
savannas as opposed to pastures.
The amount of SOC lost after the conversion of these pastures was
higher than the ones reported when rainforests were converted to OP
plantations, likely due to the high amount of SOC (102 Mg ha
−1
)
stored down to 50 cm in the studied pastures (19,20,41). This finding
is in line with those previously found in a Brazilian study, where SOC
losses were more pronounced for OP plantations derived from pasture
than from forested areas (17). However, the proportion of initial SOC
lost in this study (39%) was similar to the proportion reported for
rainforest-derived plantations, with the difference that it took longer
to reach a new equilibrium in the pasture-derived plantations (20).
The dynamics of SOC stocks after land use change is commonly
assumed to follow a single exponential decay until it reach a new
equilibrium, i.e., most losses occur within a decade after conversion
(20,42,43). In this study, losses were constant and extended over a
longer time. The initial sharp decrease followed by a stabilization
phase confirms the slowresponse of SOC to landuse changeand high-
lights the importance to assess changes in C cycling dynamics either
over longer time scales or to investigate more sensitive SOC indicators,
i.e., particulate OM, than total SOC pool size when only plantations
within the first rotation cycle are studied. The dynamics of total SOC
stocks was the net result of distinct patterns of C pool dynamics de-
pending on soil depth and C origin. The decomposition of pasture-
derived SOC did actually follow a single exponential decay in each
layer, while OP-derived SOC accumulated at constant rate, except
for 0- to 10-cm depth where SOC accumulation reached saturation.
Despite the apparent stabilizationoftotalSOCstocksdownto50cm
during the second rotation cycle, the isotopic approach demonstrated
that only the top 10-cm layer was close to the equilibrium level (Fig. 2A).
Between 10- and 30-cm depths, rates of pasture-derived C loss and OP-
derived C stabilization were similar in the oldest plantations, so that
bulk stocks appeared to have reached equilibrium. The decomposition
rate in the 30- to 50-cm layer was still faster than the stabilization rate,
explaining that the subsoil was still losing C after 56 years of OP culti-
vation. This finding is of relevance as no studies have reported, so far,
effects of land use change to OP in subsoil horizons, presumably due to
the relative short-term duration of the existent literature.
It is not possible yet to determine at which level SOC stocks will
stabilize for layers below 10-cm depth since the accumulation of
OP-derived C did not show any sign of saturation even after 56 years.
Under certain conditions, SOC stocks reach a minimum before
increasing again, as the common U-shaped reported in other long-
term SOC dynamics studies (44,45). Because the rate of pasture-
derived SOC losses decreased with time after conversion, stabilization
rates can surpass decomposition rates if the stabilization does not sat-
urate before. This mechanism can explain the recovery of C content in
the top 10 cm (Fig. 4A) and would confirm the similar tendency ob-
served for SOC stocks at least down to 20-cm depth (Fig. 2, A and B). It
is commonly observed that SOC turnover slows down with increasing
soil depth because of the higher level of SOC protection by minerals,
reduced microbial activity, or reduced root C inputs (46). Because of
slower C dynamics in deep soil, it is possible that layers below 10-cm
depth will reach the recovery phase observed in the topsoil in the third
rotation cycle. Nonetheless, it is questionable whether the soil below
30-cm depth will follow the same dynamics as the upper layer to even-
tually reach this stage (Fig. 5B). OP rooting system has a specific
architecture with fine roots growing upward to the surface from ex-
ploratory coarse roots growing horizontally at around 30-cm depth
(47). Hence, root biomass and activity are greatest in the top 30 cm.
Layers below 30 cm receive less C inputs from roots but are still
strongly enriched with nutrients leached from the heavy fertilization,
favoring SOC mineralization. Consequently, despite the stabilization
of SOC stocks during the second rotation cycle, stocks might slightly
increase or decrease in subsequent rotation cycles depending on the
intensity of the recovery in the upper layer and the stabilization level
below 30-cm depth.
Our findings demonstrate that the conversion of pasture into OP
had an important impact on SOC stocks. The most important long-
term changes in SOC storage occurred during the first OP rotation cycle
where 39% of the original SOC was lost. The second phase was charac-
terized by a redistribution of SOC within the soil profile, in which a re-
covery of SOC in the topsoil compensates for a decrease in the subsoil,
leading to a stabilization of the total SOC stocks down to 50-cm depth.
The negative impact of OP on SOC storage was high when cultivated on
pastures, but it was comparable to the impact of intensive cultivation of
other nonperennial crops on pasture or rainforests (16,26). Soil degra-
dation was mainly limited to a decrease of SOM. The typical threats
affectingsoilphysicalqualityinOPplantations established on rainforest
such as erosion and compaction were limited in the studied plantations
(19,48). Although the reference pasture soils might have been com-
pacted by trampling, native savanna soils in the Llanos region are nat-
urally compacted and thus less sensitive to further compaction (49). In
addition, the topography of the Llanosregionismostlycomposedofflat
areas (i.e., piedmont and flat high plains) reducing the risk of soil ero-
sion, contrasting with Indonesian islands where plantations are affected
by severe soil erosion (19,50).
Because of the soil preparation before OP establishment and fre-
quent fertilizer applications, inherent with low soil quality of the local
soils, soil physical and chemical fertility remained similar or even
higher after two OP cultivation cycles. Specifically, while SOC de-
clined, the sum of exchangeable bases increased during the pastures
to OP transition, implying a trade-off between soil chemical properties
and SOC in the long term. This suggests that OP nutrient supply relies
mostly on the frequent application of mineral fertilizers and not on
nutrients released from SOM mineralization by microorganisms.
Nonetheless, soils did not show signs of degradation that would pre-
vent the establishment of new crops or the restoration of (semi-)
natural plant communities following OP cultivation. This is funda-
mental because TEC changes remain theoretical since it assumes that
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OP cultivation will last permanently. Ultimately, the impact of land
use change will depend on the land use following OP. Since biomass
C stock gains disappear rapidly while SOC losses remain, the following
land use type would start with a C debt of about 40 Mg C ha
−1
in the
soil after 60 years of OP cultivation. It is, therefore, important to main-
tain soil physical and chemical properties because SOC losses from
land use change are,to a high degree, reversible (26). The sustainability
of OP cultivation would, therefore, benefit from the implementation
of management practices that incorporate organic residues, either as
empty fruit bunches, compost, or by using cover crops into the regular
soil management programs.
Soils under OP plantations in this study were far from C saturation,
as indicated by the lower SOC stocks than those found in pastures and
by the linear increase of OP-derived C observed in subsoil layers.
Therefore, a large potential for C sequestration in soils subjected to
this land use change alternative can be expected if OM inputs increase.
Furthermore, increasing SOC and nutrients in an organic form limits
the trade-off that negatively affects soil biota by increasing synergies
between soil chemical properties and SOC (51,52). Replacing soil
biological activity by mineral fertilization is risky if fertilizer costs in-
crease or if their supply decreases in the future. Moreover, soil biota
improve soil stability and resilience, facilitating the restoration of
former OP plantations (53).
Pastures tend to emit more nitrous oxide (N
2
O) emissions than
tropical forests (54); therefore, if OP will expand on pastures, then it
is plausible that this alternative land use change will compare positively
to the common deforestation scenario in terms of N
2
O emissions.
Adoption of a suite of practices for better nutrient management, i.e.,
customized fertilization programs, should be encouraged in OP plan-
tations not only to reduce mineral nutrient losses but also to limit their
stimulating effect on SOM decomposition in subsoil layers, favoring
deep SOC depletion, and reduce the greenhouse gas emission budget
from preventing N
2
Oemissions.
OP is blamed for its large environmental impacts, especially the
reduction of C stocks and biodiversity from tropical forest conver-
sion, so the search for low-impact land use change alternatives has
become imperative. This study provides empirical field-based evi-
dence that the conversion of pastures to OP is C neutral from an eco-
system C storage perspective. The availability of large pasture areas in
the tropics, particularly in LatinAmerica, could limit the negative im-
pacts of ongoing OP expansion to native savannas and natural forests
(2,14). Our findings indicate that conversion of pastures to OP can be
an opportunity to preserve and even increase C sequestration in the
tropics and reduce the large C footprint of OP development on forested
land. Recent studies on biodiversity in the Neotropics have also demon-
strated that OP plantations established on pastures can spare the devel-
opment of other ecosystems that are much richer in endemic and
threatened vertebrates (55,56).
The spatial design of OP plantations can also take greater account
of other natural land cover elements, including remnant forests and
savannas. This more heterogeneous landscape mosaic would likely
provide increased ecosystem resilience favoring both productivity
and conservation. We hope that our study will prompt research on
other fundamental aspects of OP expansion in pastures areas, such as
seasonal water scarcity and socioeconomic aspects. We recognized
that a shift in OP expansion from forested land to unproductive pas-
tures will need to be supported by policy. Improving support services,
including infrastructure development such as mills and transport fa-
cilities and facilities for the substantial labor requirements that will be
required, could encourage the development of OP in regions where
there are unproductive pastures. Further measures like banning forest
conversionor, on the consumer side, demanding effective certification
schemes for OP production would also reduce deforestation for OP
expansion and its marked environmental impacts.
MATERIALS AND METHODS
Study area
The study was carried out in “La Cabaña,”a large-scale commercial
OP plantation (73°22′W, 4°16′N) and three adjacent cattle ranching
farms, close to the town of Cumaral, of Meta Department in Colombia.
Theareaislocatedinthepiedmontof the Llanos region in the eastern
plains, close to the Andean mountains, with an altitude of 300 m (fig.
S1). The climate in the area is tropical with a well-marked dry season
that lasts from December through March. Annual rainfall is of about
3400 mm, and annual mean temperature is approximately 27°C. The
study area is located on the well-drained Pleistocene and late Tertiary
alluvial terraces, where soils are predominantly dystrophic Inceptisols
(Oxic Dystropepts) of about 60- to 70-cm effective depth overlaying
coarse alluvial sediments on flat topography.
In general, the Llanos is a vast territory mostly dominated by a
mosaic of savanna (C4 dominated) and gallery forest ecosystems that,
over the past few decades, has undergone fast land use change to in-
tensive commercial agriculture and is often regarded as one of the last
frontiers for agricultural expansion in South America (34,57). The
region accounts for about one-fourth of the national territory, respec-
tively 22 million ha (34,58). Cattle ranching is the predominant land
use in the piedmont and of the Llanos in general, where large areas
of cleared forests and savannas havebeensownwithimprovedvari-
eties of Brachiaria grasses for several decades (Brachiaria spp.) (59).
Brachiaria grasses are of African origin, and they are widely used in
improved South-American C4 pasture systems. However, during the
last 40 years, increasing areas of these pastures and natural savannas
have transitioned to intensive agriculture of rice and OP plantations.
Because of the economic and social benefits, a suit of favorable climatic
conditions in the Andean piedmont of the Llanos and increasingly
governmental stimulus, OP plantations are being established since
more than half a century, and their expansion is predicted to continue
(32). As is the case for most OP plantations in Colombia, the study site
plantations at La Cabaña were derived from pastures, which had been
planted on former well-drained grassland savannas.
Approach and study sites
We used a space for time substitution approach (chronosequence) to
quantify the long-term impacts on biomass and soil properties, in-
cluding changes in SOC stocks and soil chemical fertility character-
istics, following pasture conversion into OP plantations. As we
aimed to study the long-term effects of OP cultivation on soil proper-
ties, OP plots with palm stands passing by the first rotation cycle (up
to 30 years) and the second rotation cycle (new palms transplanted
after the first cycle) were considered. We selected six OP plots that
range from 12 to 56 years after pasture conversion and three reference
pasture sites. All OP plots were part of a large-scale OP plantation. This
large-scale OP farm could have the longest history of OP cultivation
in the whole Llanos region, and its management is representative of
the typical management of OP plantations in this region of Colombia.
The reference sites were cattle ranching farms that were adjacent to the
sampled OP farm. The primary criterion for selecting OP plots was
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the existence of pastures as the sole preceding land-use. This infor-
mation was obtained by direct communication with the personnel
in charge of both the OP farm operation and the neighboring cattle
ranching farms. In addition, in the plot selection process, sites with
steep slopes, inundated parts, or located on floodplains and with dis-
tinct management to the general farm practices were excluded. OP
plots were planted in a triangular design 9 m apart, which resulted
in a density of 143 palms ha
−1
. All OP plots, except the recently re-
planted 32-year plot, presented four well distinct management zones:
(i) the frond piles located in between palms and where pruned OP
fronds are accumulated; (ii) the harvest path, which is the area of traf-
fic for mechanized operation, i.e., fruit harvesting, in between parallel
palm lines; (iii) weeded circle, which is an area around the palm trunk
of about 5 m in diameter where most fertilizer inputs are placed up
until 5 to 6 years; and (iv) the interrow where almost no field
operationstakes place and scattered understory vegetation, i.e., weeds,
grows. Land was prepared prior plantation establishment by chisel
plow to a depth of 10 to 15 cm. Dolomitic lime was added to increase
soil pH. Fertilization practices were the typically recommended ones
for the region and were done periodically every year in two applica-
tions on the weeded circle at young ages or broadcasted all over the
plantation except the harvest path in mature plantations (over 5-year
plantations).Nitrogen(N),phosphorus (P), and potassium (K) fertiliza-
tion of 150 to 725 kg ha
−1
year
−1
were applied depending on palm stand
age, i.e., 725-kg NPK-complete fertilizer applied to plantation aging
more than 10 years. Other nutrients including boron and magnesium
were also applied regularly every year.
Site selection and sampling
Soil samples were taken from a chronosequence of OP with stand
ages of 12, 18, 30, 32, 45, and 56 years, the three first blocks cor-
respond to first cycle plantations and the last three to second cycle
plantations. OP blocks were of sizes between 20 and 30 ha. In addi-
tion, three adjacent cattle ranching farms were sampled as reference
sites. All selected sites were located within an area that covered
roughly 5000 ha.
Soil samples from OP plots were collected using a modified tran-
sect methodology (60). This sampling strategy allows us to have
mixed samples that represent well the spatial variability in OP plan-
tations due to management practices. Furthermore, it is also well
adapted for measures in replanted plantations, since the spatial
distribution of management zones differs between OP cycles. Twenty
sampling points evenly spaced were marked along a 50-m diagonal
transect at ca. >60° (considering a selected palm at row 1 of the transect
as reference point). The diagonal transects crossed six OP rows, and
the four management zones were typically found in commercial OP
plantations. To capture the spatial variability at each of the OP blocks,
three parallel transects were made, except in the 12- and 32-year OP
blocks, and sampled in 2016, with some complementary sampling in
2017. One transect was established in a centered position relative to
the number of palm rows and average number of palms per row in
each block. The other two transects were established at least 120 m
away from each side of the first transect. Transects were established
at least 50 m away from the plot’sedges.AtthethreeBrachiaria pasture
sites, one diagonal transect of 50 m long oriented east-west with
20 evenly spaced sampling points was made. At all diagonal transects
(OP blocks and pasture sites), a total of 20 soil cores were taken. Half
of those cores were taken to a depth of 30 cm and the other half went
down to 50 cm in an alternative manner, using a 6-cm-diameter soil
auger. Cores were divided into four depth intervals: 0 to 10 cm, 10 to
20cm,20to30cm,and30to50cm.Therefore,samplesofthe0to
10 cm, 10 to 20 cm, and 20 to 30 cm were composed of 20 cores, and
the 30- to 50-cm samples were made of 10 cores. Final samples in each
transect were bulked into a composite sample, resulting in one sample
for each depth in each transect. Samples were homogenized, air-dried,
sieved through 2 mm, sealed in bags, and stored at room temperature
until transportation to the laboratory in Lausanne (Switzerland). Soil
physical, chemical, and isotopic analyses were carried out after drying
at 35°C in forced-air ovens.
Pits were dug in a middle representative position along the first
50-m linear transects to determine soil BD in each OP block and
one reference site to 70-cm depth. Two stainless steel volume cores
were inserted horizontally into a pit wall at each depth increment.
Soils from the two cores were mixed and oven-dried at 105°C for
48 hours to calculate BD.
Above- and belowground biomass
At the previously described central diagonal transects of each OP
sampled plot, the heights of 10 randomly chosen palms were mea-
sured. Palm height was measured from the palm base to the base of
the youngest fully expanded leaf (61). Estimation of aboveground
biomass was based on palm height using the allometric equation for
mineral soils (37)
AGB OP ¼0:0923ðheightÞþ0:1333 ð1Þ
Belowground OP biomass was estimated according to the allomet-
ric model based on OP plantation age (Eq. 2) (62)
BGB OP ¼1:45 ðageÞþ9:88 ð143 palms ha1Þð2Þ
Biomass C stocks were estimated using a factor of 41.3% of above-
and belowground OP biomass (62). Time-averaged C in OP biomass
was estimated as the C stocks accumulated in the middle of one rota-
tion cycle; thus, the biomass C stock in a 30-year-old OP plantation
was divided by two (63).
Laboratory analyses
Soil particle size analysis was performed on air-dried soils by the
hydrometer method after removal of organic fraction with 30%
H
2
O
2
(64). Soil pH was determined in a 1:2.5 soil-to-water slurry.
Soil samples were extracted with Mehlich-III solution (65) and ana-
lyzed for available cations including Ca, K, Na, and Mg using an
inductively coupled plasma spectrometer (PerkinElmer, Waltham,
MA, USA). Exchangeable acidity was determined by extracting 2 g of
soil with 10 ml of 1N KCL, shaking for 30 min at 200 rpm. Samples
were allowed to settle for 30 min, and filtered, and extraction funnels
were washed three times with 30 ml of 1N KCl. Titration was con-
ducted with 0.01N NaOH after adding phenolphthalein to the extract
(66). Effective cation exchange capacity (ECEC) was estimated by
summing the amount of charge per unit soil (meq 100 g
−1
)frommajor
cations (Ca, K, Na, and Mg) plus exchangeable acidity. BS was ob-
tained by dividing the total sum of charge per unit soil from Ca, K,
Na, and Mg by ECEC.
Total C and N contents,
13
C, and
15
N were measured on air-dried
and ground soil weighted in tin cups with an Elemental Analyser
(EuroVector) coupled to an isotope ratio mass spectrometer (Delta
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plus, Thermo Fisher Scientific) at the stable isotope lab at the Swiss
Federal Institute for Forest, Snow and Landscape Research WSL,
Birmensdorf, Switzerland. Total C content corresponds to total organic
content because of the absence of carbonates in heavily weathered soils.
The SOC stocks were calculated as the product of soil BD, layer
thickness, and SOC concentration. The contribution of new and old
C to total SOC was calculated as shown in Eq. 3 (67)
f¼ðdsam drefÞ=ðdop drefÞð3Þ
where fis the relative proportion of OP-derived C (C3) in SOC
stocks. dsam is the d
13
C of the soil sample, and dref is the d
13
Cof
the corresponding soil depth from pasture as C4 reference soil.
dop is the d
13
C of nine fine root biomass C samples. The method
accounts for the natural increase of d
13
C signature with depth gen-
erally observed in soils and neglects the
13
C fractionation that could
occur at the first step of SOC formation.
Statistical analyses
Data analyses were performed using RStudio version 3.4.0 (R Devel-
opment Core Team 2017) statistical software. Linear regression anal-
ysis was used to examine changes in soil chemical and physical
properties (i.e., major cations and BD) relative to increase time after
pasture conversion into OP plantations. Assumption of normality
was checked for all analyses with Shapiro-Wilk test and visual in-
spection of normality plots. If assumption of normality was not
satisfied, then permutation tests were performed as in the case of
Ca, sum of cations, and BS. Patterns in changes of soil C stocks over
the OP chronosequence time were examined for the bulk soil and for
each of the four sampled soil layers using regression models. The
nonlinear least square “nls”and linear model “lm”functions in R
were used to fit nonlinear and linear regression models, respectively.
In addition, the “segmented”function was used to perform seg-
mented (broken line) regression analysis. Statistical significance was
declared at P< 0.05. Similarly, model fit for changes in C3-OP–derived
C and C4 pasture–derived C over the chronosequence time was also
examined for each of the four studied soil layers by testing the above-
mentioned models. These regression analyses allowed estimating rates
of C3 accumulation and C4 decomposition and decay constants (k),
rates of total soil C decrease, and break points in soil C stock changes
(time at which a change in the direction of change in C stocks
occurred).
After testing various models (i.e., mono-exponential and bi-
exponential), model performance assessment was based on Akaike
information criterion (AIC) and coefficient of determination (R
2
)
values. Models with the largest R
2
and lowest AIC values were selected
(see table S1). Accordingly, (i) changes in whole soil C stocks and C
stocks in each soil layer were described by fitting segmented regression
models (except linear regression on the deepest soil layer of 30 to
50 cm), which yielded estimated break points; (ii) C3-derived C in
the 10- to 20-cm, 20- to 30-cm, and 30- to 50-cm soil layers were
described by linear models, while pattern in C3-derived C in the
soil surface layer (0 to 10 cm) was described by an exponential rise
to equilibrium model of the form
y¼ðk*y0AÞ*expðktþAÞ=kðð4Þ
where yis the C stock, kis the annual decay constant of the pool, y0is
the C3-C stock before OP cultivation started (thus, 0), Ais the C3
annual input to the C3 pool, and tis time after conversion; (iii) A
first-order decay model was fitted to the obtained pasture-derived
C data in the four studied soil layers
y¼c*expðktÞð5Þ
where yis the C stock, cis the original C stock before OP cultivation,
kis the decay rate constant, and treferred to time. The half-life (HL)
of the original C stock in Eq. 5 and of the OP input in Eq. 4 was
calculated as
HL ¼lnð2Þ=kð6Þ
A PCA was carried out for further exploration of the relations
between soil parameters that can be affected by cultivation (BD, C:N,
13
C, C, N, EA, Na, pH, K, Mg,
15
N, Ca, BS, and P).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/5/11/eaaw4418/DC1
Fig. S1. Map of study sites and the potential area for the expansion of OP in pasture lands in
the Neotropics.
Table S1. Set of models tested for the bulk soil and pasture- and OP-derived carbon.
Table S2. Soil chemical, physical, and isotopic properties.
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Acknowledgments: We are grateful to the following persons of Hacienda La Cabaña S.A.
for granting us access to field work, information, and hospitality: J. Zambrano, Y. Mejia, W. Mican,
C. Colmenares, and others. We are also thankful to R. Schlaepfer and P. Mariotte from
ECOS laboratory for the support in statistical analysis. Funding: This work was financed
by the Swiss National Science Foundation (r4d-Ecosystems) “Oil Palm Adaptive Landscape”
no. 152019. Author contributions: T.G., J.C.Q., and A.B. conceived and designed the study.
SCIENCE ADVANCES |RESEARCH ARTICLE
Quezada et al., Sci. Adv. 2019; 5: eaaw4418 20 November 2019 10 of 11
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A.E. contributed to field work. J.C.Q. carried out the research assisted by T.G. J.C.Q. performed
the statistical analysis with contributions from T.G. and A.B. J.C.Q. prepared the manuscript with
contributions from all authors. T.G., A.B., A.E., and J.G. revised the manuscript. Competing
interests: All authors declare that they have no competing interests. Data and materials
availability: All data needed to evaluate the conclusions in the paper are present in the paper
and/or the Supplementary Materials. Additional data related to this paper may be requested
from the authors.
Submitted 20 December 2018
Accepted 18 September 2019
Published 20 November 2019
10.1126/sciadv.aaw4418
Citation: J. C. Quezada, A. Etter, J. Ghazoul, A. Buttler, T. Guillaume, Carbon neutral expansion
of oil palm plantations in the Neotropics. Sci. Adv. 5, eaaw4418 (2019).
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on November 21, 2019http://advances.sciencemag.org/Downloaded from
Carbon neutral expansion of oil palm plantations in the Neotropics
Juan Carlos Quezada, Andres Etter, Jaboury Ghazoul, Alexandre Buttler and Thomas Guillaume
DOI: 10.1126/sciadv.aaw4418
(11), eaaw4418.5Sci Adv
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REFERENCES http://advances.sciencemag.org/content/5/11/eaaw4418#BIBL
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