Agriculture, Ecosystems and Environment 171 (2013) 7284

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Agriculture, Ecosystems and Environment

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Carbon stocks and accumulation rates in tropical secondary forests at

the scale of community, landscape and forest type
D.E. Orihuela-Belmonte a , B.H.J. de Jong a, , J. Mendoza-Vega a , J. Van der Wal b ,
F. Paz-Pellat c , L. Soto-Pinto d , A. Flamenco-Sandoval d
a

El Colegio de la Frontera Sur, Av. Rancho Polgono 2A, Parque Industrial Lerma, Campeche, Camp CP 24500, Mexico
El Colegio de la Frontera Sur, Carretera Villahermosa-Reforma km 15.5, Ranchera Guineo, seccin II, Villahermosa, Tab CP 86280, Mexico
c
Colegio de Postgraduados, Carretera Mxico-Texcoco Km. 36.5, Montecillo, Texcoco, Edo de Mxico CP 56230, Mexico
d
El Colegio la Frontera Sur, Carr. Panamericana y Perifrico Sur s/n, Barrio Mara Auxiliadora, San Cristbal de Las Casas, Chis CP 29290, Mexico
b

a r t i c l e

i n f o

Article history:
Received 5 July 2012
Received in revised form 12 March 2013
Accepted 13 March 2013
Available online 21 April 2013
Keywords:
Carbon stocks
Carbon accumulation rates
Forest chronosequence
Land-use intensity.

a b s t r a c t
Rapid increases of secondary forest areas in the tropics make understanding of their carbon dynamics
critical to estimate net CO2 emissions and uptake. This understanding is needed for performance based
mechanisms that aim to halt global warming (REDD+). Despite the importance of secondary forests to
global C cycling, the impacts of recovering secondary vegetation on C dynamics are poorly understood.
We present carbon stocks and accumulation rates in biomass and soil pools, using as a basis of analysis 87
sampling plots established along a secondary forest chronosequence derived from shifting cultivation.
We test the inuence of age, land-use intensity (prior land-use history) and two site quality indices on
the size of the C stocks and C accumulation rates. Biomass and Total C pools were positively correlated
with age and negatively with LU intensity, whereas C accumulation rates had opposite signs for both
parameters. Soil C did not show any variation along the age gradient, but C in the upper 20 cm was
positively correlated to both site quality indices. The LU-intensity inuenced the tree C stock in the
younger plots. We propose a nested approach in which detailed studies can be up-scaled to landscape
and regional estimates of carbon pools in forest fallow and undisturbed forests and carbon accumulation
rates in forest fallow.
2013 Elsevier B.V. All rights reserved.

1. Introduction
Rapid increases in secondary forest cover have been reported
for the tropics, primarily as a result of anthropogenic disturbances
(Brown and Lugo, 1982; Skole and Tucker, 1993; FAO, 2010). At the
end of the 20th century, secondary forests already accounted for
roughly 60% of tropical forested areas (ITTO, 2002). Understanding the dynamics of tropical secondary forests is becoming critical
for the development of tropical forest management and conservation strategies worldwide, given that these can be considered the
forests of the future (Wright, 2005; Sanchez-Azofeifa et al., 2005),
if historical trends of land-use change continue. The existing pattern of land-use change is creating a complex landscape consisting
of agricultural elds, pasture lands, secondary forest patches with
different histories of disturbance and succession, and fragments of
old-growth forests.

Corresponding author. Tel.: +52 981 1273720x2413;

fax: +52 981 1273720x2001.
E-mail address: bjong@ecosur.mx (B.H.J. de Jong).
0167-8809/$ see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.agee.2013.03.012

Secondary forests have always been part of the dynamics of

small-scale natural disturbances in tropical forest ecosystems, such
as tree fall due to senescence, strong winds or forest res, where
subsequent succession is key to restoring the structure and function of old-growth forest. However, large-scale land-use change
dynamics, such as conversion to slash-and burn agriculture and
pasture land, alter the structure and function of forest ecosystems (Read and Lawrence, 2003; Lawrence, 2005; Lawrence et al.,
2007), which feeds back on their carbon (C) balance. Tracts of secondary forests emerge where agricultural or pastoral land use is
discontinued. The secondary forest on the abandoned agricultural
elds re-accumulate ecosystem C (Hughes et al., 1999; MarinSpiotta et al., 2008). Estimates of net CO2 emissions in areas where
slash-and-burn agriculture is common practice need to take into
account the C dynamics in secondary forests, as these forests are
an important C sink following the original losses associated with
clearing. Impacts vary according to the type of event, its intensity
and frequency. Previous studies report rapid rates of aboveground
biomass accumulation during the initial stages of succession of
about 100 Mg/ha in the rst 15 years of succession (Ewel, 1980;
Lugo and Brown, 1992). As such, secondary forests have the potential to restore large amounts of C that were lost during deforestation

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

and can thus play an important role in sequestering atmospheric

CO2 (Kauffman et al., 1995).
Already in 1980s, tropical secondary forest occupied around
600 106 ha (35% of total forest; Brown and Lugo, 1990). FAO estimated the area occupied as shifting cultivation around 360 106 ha
in the early 1980s (FAO/UNEP, 1982), which represents about 30%
of all exploitable soils. In Mexico, the area classied as secondary
tropical lowland forest amounted to 19.3 106 ha in 2002 (64.5% of
all tropical lowland forest), of which 12.4 106 ha are considered
as part of the shifting cultivation cycle (INEGI, 2005).
Assessments of the carbon dynamics in tropical secondary
forests that develop after abandoning agricultural practices are still
rare (Hughes et al., 1999, 2000; Markewitz et al., 2004; Eaton and
Lawrence, 2009; De Jong et al., 2010). The potential for tropical
forests to remove C from the atmosphere and store it effectively
depends on net primary productivity, the allocation of C to the living plant reservoirs (leaf, branch, stem, root), and the residence
time of C in the living and dead reservoirs (litter, dead woody debris,
soil organic carbon, etc.). A major limitation for our understanding
of how forests recover after abandoning agricultural activities, is
the short time available for its study relative to the generally longer
time span over which the process takes place (usually decades).
Uncertainties in the rates of secondary forest growth are critical
data gaps limiting our understanding of the role of tropical forests
as sources and sinks of atmospheric CO2 (Asner, 2011; De Jong et al.,
2010).
Successful design and implementation of strategies designed to
reduce emissions through the forestry sector requires an understanding of C dynamics including both the size of C pools and the
rates of C loss or accumulation (Kanninen et al., 2007). More precise data on carbon stocks and carbon stock change over time are
of particular interest for countries like Mexico in the light of possible future nancial mechanisms that are discussed in relation
to reducing emissions from deforestation and forest degradation,
or managing and enhancing carbon stocks (REDD+). Currently,
ve options are considered for national REDD+ approaches. Two
options require information on the size of carbon stocks: reduced
deforestation and stock conservation. Three options will require
additional data on carbon stock changes over time: reduced forest degradation, sustainable forest management and carbon stock
enhancements (Herold and Skutsch, 2011). REDD+ is a proposed
performance-based mechanism, in which developed countries
compensate developing countries for forest emissions reductions
through a variety of anticipated nancial mechanisms, working at
different scales (Phelps et al., 2010).
A key question in the international debate concerns the level
(scale) at which accounting should be carried out and incentives offered for REDD+ activities (see Angelsen et al., 2009). The
scale for accounting of REDD+ mitigation potential has implications for the effectiveness, efciency and equity of the REDD+
nancial mechanisms (Wertz-Kanounnikoff and Angelsen, 2009;
Vatn and Angelsen, 2009). It is expected that in most countries
activities will be implemented at community level. A performancebased system of carbon management through community-level
activities will require their accountability at the local scale to be
transparent and coherent with national accounting (Corbera and
Schroeder, 2011) through some type of nested approach (Cortez
et al., 2010). Research should therefore focus on how carbon
sequestration estimations can be developed that can be scaled from
community-based mitigation measurements, through landscapelevel assessments to national-scale accounting.
Due to the increased extent of tropical secondary forests,
enhancement of forest carbon stocks should be considered as a
major component in the future negotiations of REDD+ (Edwards
et al., 2010), for which not only stock data are required but also
estimation of stock change over time (carbon accumulation rates).

73

At a local scale, carbon accumulation rates in secondary forests

may vary according to age (time after abandonment; Read and
Lawrence, 2003), land-use history (number of times converted to
crop land; Van der Wal, 1999; Eaton and Lawrence, 2009), local site
conditions (environmental conditions, physical and chemical characteristics of soils; Batjes and Sombroek, 1997; Feller and Beare,
1997; Lorenz et al., 2009) or a combination of both. To analyze
the rates at the landscape level, it is expected that the main factor
inuencing the carbon accumulation rate will be the area occupied
by secondary vegetation, its age structure and LU-history (Eaton
and Lawrence, 2009), whereas for national accounting the amount
of secondary forest will be the most important parameter used to
estimate carbon accumulation rates (De Jong et al., 2010).
In this paper we present the results of a study that collected data
on C pools in a Mexican tropical secondary forest chronosequence.
We used data collected in 87 plots spread to quantify the carbon
stocks and rates of accumulation in living and dead biomass and
soil pools, and to evaluate the inuence of factors such as age, site
quality and land-use intensity (prior land-use history) on the size
of the stocks and accumulation rates. We examined the combined
inuence of these factors on the magnitude and rate of change of
the C pools (vegetation, dead wood, litter, soil) in a secondary forest
chronosequence. Finally we propose a nested approach in which
detailed studies, such as presented in this paper, can be up-scaled
to landscape and regional estimates of carbon pools in forest fallow
and undisturbed forests and carbon accumulation rates in forest
fallow.
2. Methods
2.1. Study area
The study was carried out in the El Ocote Biosphere Reserve,
located in the north-eastern part of Chiapas, Mexico, between
16 45 42 and 17 09 00 North and between 93 54 19 and
93 21 20 East. The reserve extends about 100,000 ha, of which
around 40% is completely protected, whereas the remaining 60% is
considered as buffer zone with high conservation importance due
to the high number of endemic species (Fig. 1). The whole area is
part of the Meso-American Biological Corridor (CONANP, 2000). The
reserve is located between two neo-tropical provinces, the Pacic
and Tehuantepec, characterized by a highly varying topography
with altitudes between 180 and 1300 m. a.s.l. The climate is tropical
humid (20002500 mm yr1 ) to subhumid (15002000 mm yr1 ).
The area is characterized by a karstic landscape with its sinkholes, hills, eld depressions and caves (Mulleried, 1957). The soils
are predominantly of alluvial origin, sedimentary rocks, limestone,
sandstone, mudrock, limonite, intrusive rocks and conglomerates
(Leptosols, Luvisols and Regosols). The original vegetation is tropical evergreen and semi-evergreen rainforest. Colonization of the
area started in the 1970s and since then part of the original forests
has been converted to secondary forests and agricultural land due
to slash-and-burn agriculture. This type of agricultural production is a cyclic system that includes a short period of corn and
bean cultivation followed by a fallow period that formerly lasted
about 10 years, but which in recent years has often been reduced
to two to four years due to land-use intensication (CONANP,
2006).
2.2. Sampling
We established 87 monitoring plots of 1000 m2 in mediumstature semi-evergreen rainforest in seven communities located
around the border of the biosphere reserve. Of these, 63 plots were
located in forest fallows recovering between 1 and 40 years from
cultivation, and 24 in undisturbed forests (Fig. 1).

74

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

Fig. 1. Location of study area and sampling plots.

The time recovering from cultivation (fallow age) and the number of cultivation cycles was determined by means of interviews
with the landowner and crosschecked with observations in the
eld of signs of cutting (such as bifurcations of trunks and girth
of lateral branches). The dates were referenced with data obtained
in community assemblies on important historical events, like the
foundation of the community, legal recognition of land rights,
severe forest res, and years of national elections. Sites were
selected according to age and condition: relatively homogeneous
vegetation on a squared continuous area larger than 1 ha. Data were
collected in a circular plot of 1000 m2 , located in the center of the
area. The circular plots were corrected for slope. We measured DBH
(Diameter at Breast Height, 1.30 m) and total height (H) of all trees
with DBH > 10 cm. In the inner central circle of 100 m2 we measured
DBH and height of all trees with DBH > 2.5 cm. To estimate the dry
weight of above ground biomass (AGB) of each tree, we used the
allometric equation developed by Cairns et al. (2003) for forests of
similar characteristics in the Yucatn Peninsula (Eq. (1)).

AGB = exp 2.172 + 0.868 ln(DBH2 H) +

0.0939
2


(1)

where AGB is in kg dry weight, DBH in cm, and H in m.

Biomass of dead trees was estimated with the same formula,
multiplying AGB with a factor of 0.5 (Eaton and Lawrence, 2009).
Root biomass was estimated with Eq. (2) (Cairns et al., 1997).
Root Biomass = exp(1.0587 + (0.8836 ln(AGB))

(2)

where ln(AGB) is the natural logarithm of above-ground biomass.

A factor of 0.45 was used to convert above-ground and root
biomass to carbon (Brown and Lugo, 1982; Brown, 2002; this
paper).
Non-tree biomass was harvested in four 1 m2 randomly distributed subplots within the 1000 m2 plots. Fresh weight was
determined in the eld and dry weight in the laboratory after

drying for 72 h at 70 C. Carbon content of leaves, fruits, owers, and branches was measured in the laboratory according to
standard procedures (IPCC, 2003). Litter was collected in 4 circles of 0.07 m2 each, separated in three layers: freshly fallen,
dry litter and humus. All litter material was oven dried for 72 h
at 70 C. C-content was determined in the laboratory of samples of the collected material. Fallen woody debris was measured
along 4 lines of 25 m length, applying the line-intersect methodology (Brown and Roussopoulos, 1974; Valentine et al., 2008) and
recorded in 4 separate decomposition classes: fresh with leaves
attached, without leaves and bark rmly attached to branch, bark
falls off after hitting, branch falls apart after hitting. Dead woody
debris in this study comprises the sum of dead standing trees
and fallen woody debris. Samples were collected in each class of
fallen woody debris to determine relative density and C-content
in the laboratory. Soil composite samples were taken for three
depth intervals (010, 1120 and 2130 cm) from soil collected
at 8 points at each site, and soil bulk density (cylinder method,
Green and Fordham, 1975) and C-content were determined for each
depth class (Eriksson and Holmgren, 1996). C-content of plant and
soil samples were determined with a 5000A Shimadzu analyzer,
using standard laboratory procedures (AOAC, 1980; CSTPA, 1980;
Anderson and Ingram, 1993). Since the soils were generally shallow and irregular in depth, soil depth was measured in 144 points
in each site and C-content of the soils was adjusted to the estimated volume of the soil at each depth interval derived from the
144 points.
Land-use intensity was calculated using the number of times
the plot was cultivated in the past, the number of years cultivated
and in fallow during each cycle (Eq. (3)), which we adapted from
Young (1994). A cycle is referred to the sum of years in cultivation
plus years in fallow.
LU-Intensity = t

C
(C + F)

(3)

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

75

Table 1
Parameters and values used to calculate the site quality indices.
Parameter

Value

Site Quality 1
Nitrogen content (%)
Phosphorous content (ppm)
Cation exchange capacity (cmol kg1 )
Calcium carbonate content (%)
pH
Soil texture

Site Quality 2
Percent of area covered by rocks
Position on hill side
Origin of re
Slope (%)
Average soil depth
(5 cm classes)

<0.032
<15
<5.0
05
<5.5
Sandy
6
Sandy clay loam

0.0320.099
15.130
5.115
5.110
5.66 or >8.3
Clayey

0.100.158
>30
15.120

0.1590.221

>0.221

20.140

>40

7.48.3
Sandy clay
7
Clay loam

6.17.3
Silt loam

50100%
Top
Intentional
50%
05 cm
6
25.130

2650%
Medium
Natural
4050%
5.110

1125%
Bottom
No re
3039%
10.115

110%
Flat

0%

2029%
15.120
7
>30

019%
20.125

where LU-Intensity is the land-use intensity; t is the number of

cycles; C is the years in cultivation in each cycle; F is the years
under fallow in each cycle.
We developed two site quality indices (Table 1), one derived
from chemical and physical characteristics of the soil sample (Site
Q1) and one derived from a series of visible parameters recorded
in each plot (Site Q2). The chemical and physical characteristics
of the soil samples included in Site Q1 are: nitrogen content (%),
phosphorous (ppm), Cation Exchange Capacity (CEC; cmol kg1 ),
considering that CEC values below 5.0 cmol kg1 indicates a degree
of infertility and higher CEC indicates better availability of nutrients (FAO, 1979), Calcium Carbonate (%), considering that in the
presence of carbonate the clay complex is dominated by exchangeable Ca, which in turn favours soil physical conditions, pH, taking
into account that most plant nutrients are best available in a neutral pH (Landon, 1991), and soil texture, where we consider mainly
the water availability and drainage capacity. The Site Q1 was calculated separately for each soil depth (010, 1120, 2130). The
environmental variables taken into account in Site Q2 include: percent of area covered by rocks, position on hill side, slope, origin of
re (induced or natural), and average soil depth in 5 cm classes.
The scores of each factor were summed for each plot, with
the nal score of Site Q1 theoretically ranging from 6 (all values 1; lowest site quality) to 27 (all values at max; highest site
quality) and with the nal score of Site Q2 ranging from 5 (all values 1; lowest site quality) to 19 (all values at max; highest site
quality).

Silt loam
8
Frank

In Table 2 we present the average, maximum and minimum values of LU-intensity, Site Q1 and Site Q2 for each forest fallow age
class and undisturbed forest. As expected, the average LU-intensity
index decreases from the low to high age categories, as older vegetation is indicative of a less frequent use of land for agriculture,
taking into consideration that the area has been colonized for only
about 40 years. Site Q1 and Site Q2 do not show a systematic difference between low and high age categories.
2.3. Statistical analysis
The C-pools were analyzed independently and in combination:
carbon (C) in living tree biomass (TreeB) is combined with C in
living non-tree biomass into C in total living biomass (TLB); C in
TLB combined with C in dead biomass (woody debris and litter)
into C in total living and dead biomass (TLDB), C in TLDB with
soil carbon into Total C. Stocks of the pools were calculated for
each plot. Average increments of C in living and dead pools were
estimated for each plot, dividing the pool sizes by the number of
years of recovery for C in living tree biomass (TreeB Incr), total living biomass (TLB Incr), and total living and dead biomass (TLDB
Incr).
We tested for differences in stocks and accumulation rates
at three levels of plot aggregation: (1) all forest fallow plots
aggregated together versus plots located in undisturbed forest,
(2) the forest fallow plots grouped in age class categories and
(3) multiple linear regression analysis with age, LU-intensity

Table 2
Average, maximum and minimum values of Land-use intensity and site quality indices.
Age class

Number of plots
Land-use intensity
Average
Max
Min
Site Quality 1
Average
Max
Min
Site Quality 2
Average
Max
Min

Undist. forest

05

610

1115

14

15

13

1.12
2.57
0.40

0.73
1.60
0.40

0.40
0.64
0.12

1620

2125

2630

3140

24

0.25
0.40
0.11

0.19
0.32
0.04

0.06
0.12
0.03

0.03
0.03
0.03

n.a.
n.a.
n.a.

20.3
23
18

20.7
24
18

20.1
23
17

21.2
24
19

19.5
22
16

21.8
24
19

19.0
22
16

18.8
22
16

12.3
18
7

9.3
13
6

9.5
17
7

10.0
13
9

9.7
14
7

12.7
18
10

9.7
13
6

10.7
15
8

Undist. Forest, undisturbed forest; n.a., not applicable; max, maximum value observed; min, minimum value observed.

76

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

and site qualities of each plot as independent continuous variables. These levels correspond to the scale for which the results
can be applied: forest fallow versus undisturbed forest at the
regional scale of forest type and climatic conditions, age classes
for landscape-level analysis and multiple regression equations to
be applied for small-scale community-level estimations. These
scales also correspond to the sources of data generally available or
obtainable.
We performed an analysis of variance (ANOVA; p < 0.05)) to
test which pool stocks were signicantly different between forest
fallow and undisturbed forest. Soil Organic Carbon was logtransformed to t the ANOVA assumptions. We could not t the
dead biomass pools to the ANOVA assumptions, therefore dead
biomass results should be interpreted with caution. All other pools
met the ANOVA assumptions. We estimated average TreeB Incr, TLB
Incr and TLDB Incr combining the data of all forest fallows and estimated their respective 95% condence intervals. Next, we grouped
the plots from 1 year to 30 years in six 5-year classes and secondary plots of 3140 years in one class. We applied an ANOVA
and Tukeys honest signicant difference test (p < 0.05) to separate
homogeneous groups of age classes in relation to each pool and
sum of pools, grouping these in living biomass (TLB), dead biomass
(TDB), living and dead biomass (TLDB), soil organic carbon (SOC)
and total carbon (Total C), and accumulation rates TreeB Incr, TLB
Incr, and TLDB Incr. Lastly, we analysed the linear effects of age as a
continuous variable, LU intensity and site qualities Q1 and Q2 on the
pools and accumulation rates, and performed a forward stepwise
generalized regression procedure to select one or more of these predictor variables to explain the size of the carbon stocks and carbon
accumulation rates. The most signicant regression models with a
total probability of rejection of less than 1% were selected. Using
this approach, the selected models may contain a non-signicant
explaining variable, which in these cases is indicated in the results.
The latter analysis is expected to improve the explanation of local
variation in carbon dynamics. We derived the recovering time
required for a fallow to reach the biomass density of undisturbed
forests using the relationship between biomass density and age.
We discuss the application of the results at local, landscape and
regional scale and how to integrate these with results, obtained
from similar studies in other parts of southern Mexico.

3. Results
3.1. Carbon content of the pool components
The carbon content of the pool components varied between
48% in fresh woody debris to 27% in humus. Fresh leaves had a
slightly higher C-content than fresh branches. The C-content in
both litter and woody debris show a downward trend according
to decomposition stage: in litter the C-content decreased from 39%
to 27% from fresh litter to humus and in woody debris from 48%
to 36% from freshly fallen branches to branches falling apart after
hitting (Table 3). We used the average C-content of fresh woody
debris (48%) and fresh branches (42%) to convert biomass to carbon
content.

Table 3
Carbon content of the pools analyzed.
Pools

C (%)

CI (%)

Fresh litter
Dry litter
Humus
Ds1
Ds2
Ds3
Ds4
Fresh branches
Fresh leaves

87
87
87
70
65
45
40
87
87

39
36
27
48
45
41
36
42
44

2.3
4.2
7.1
1.8
2.2
2.8
7.9
1.1
0.8

N, number of samples; C (%), Average carbon content; CI, 95% condence interval in %
of the mean; Ds1 , fresh woody litter with leaves attached, Ds2 , woody litter without
leaves and bark rmly attached to branch, Ds3 , woody litter with loose bark, Ds4 ,
woody litter with branch falling apart after hitting.

3.3. Carbon pool sizes in secondary forest versus primary forest

Comparing the pools of all secondary forests as one class with
the pools of undisturbed forests, the stock of C in trees and litter were signicantly higher (p < 0.05) in undisturbed forests, with
almost twice the amount of C in trees and almost 50% more in litter.
All pool combinations that include tree biomass were signicantly
higher (p < 0.05) in undisturbed forests compared to secondary
forests (Table 4). It is noteworthy that total soil organic carbon
(SOC) was very similar in undisturbed forest compared to secondary forest.
3.4. Variation of carbon pool sizes amongst age classes
Tree carbon increased from 24 Mg C ha1 in the age class 15
year to 104.9 Mg C ha1 in forests of 2630 years old. Dead woody
debris (DWD) shows a variation in mean pool size without statistically signicant differences (p < 0.05) between the age classes.
The pool size ranged from 0.8 Mg C ha1 (age class 1620) to
6.7 Mg C ha1 in the age class 3140, similar to the amount of C
in DWD of undisturbed forest and no signicant difference could
be observed among the age classes (Tables 4 and 5). Litter Cdensity also varied little among age classes with no signicant
differences (p < 0.05) among the age classes. The pool size varied from 6.4 Mg C ha1 in the age class 2530 to 10.1 Mg C ha1 in
undisturbed forests (Tables 4 and 5). Soils in Karstic landscapes
commonly have high carbon content in % of volume (Mendoza-Vega
and Messing, 2005; Fig. 2), but they are usually shallow and present
a high density of rocks on the surface. Due to these characteristics, total SOC stock (in Mg C ha1 ) in the study sites was relatively
low, varying between 62.3 and 91.9 Mg C ha1 with around 50% of
total SOC in the rst 10 cm in all age classes (Table 5). The total

3.2. Carbon content in soil

Carbon content (in % of volume) in the soil prole varied
between 3% and 10% and was highest in the 010 cm layer and
lowest in the 2130 cm for all age classes, as expected. No significant differences (p < 0.05) in any of the three depth classes could
be observed between age classes, due to the high variation in each
prole and age class (Fig. 2).

Fig. 2. Soil organic carbon content (% of volume) in each depth layer and age class.

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

77

Table 4
Average carbon content (Mg C ha1 ) in the main pools of forest fallow and undisturbed forests in the Ocote, Mxico.
Secondary forest n = 63
Tree biomass (TreeB)
Total living biomass (TLB)
Litter
Total dead biomass (TDB)
Living + dead biomass (TLDB)
Soil organic carbon (030 cm)
TotalC

59.29
60.26
7.46
11.08
71.34
74.93
155.37

(8.96)
(8.99)
(0.84)
(1.83)
(9.63)
(+9.8; 8.7)
(12.78)

Undisturbed forest n = 24

Sign. Diff.

104.03
105.29
10.13
16.71
121.99
74.80
191.47

*
*
*
*
*
N.S.
*

(14.52)
(14.56)
(1.37)
(2.97)
(15.61)
(+12.2; 10.5)
(16.80)

*p < 0.05; between parenthesis 95% condence interval. Soil organic carbon derived from log-transformed average and condence interval.

mean carbon density in the age classes varied between 115.4 Mg C

in forests of 15 years old, to 211.5 Mg C in forests of 2530 years
old. The contribution of tree biomass to total C-content in the forest
ecosystems varied between 21% in young secondary forests to 53%
in undisturbed forest (Tables 4 and 5). The magnitude of the other
C pools varied little in absolute terms, although their proportion of
total C decreased along the age gradient, as carbon in tree biomass
increased.

3.5. Correlation between carbon pool size and accumulation rates

in relation to age, LU-intensity and site qualities
All biomass carbon pools were positively correlated with age
(Table 6). TreeB, TLB, TLDB, Total C were negatively correlated with
LU-intensity, whereas TreeB, TLB, and TLDB were also negatively
correlated with Site Q1 (chemical and physical soil characteristics).
A positive correlation was observed between Total C and site Q2
(environmental characteristics). Both DWD and litter C stocks were
positively correlated with age, whereas DWD was negatively correlated with LU-intensity. Site Q2 was only positively correlated
to all living and soil pools in undisturbed forest (p < 0.05; results
not presented). SOC content in the rst 20 cm is positively correlated with both site quality indices, whereas SOC at 2130 cm depth
was only positively correlated to Site Q2. All calculated accumulation rates were negatively correlated with age and positively with
LU-Intensity, whereas all rates that include tree biomass (TreeB

Incr, TLB Incr, and TLDB Incr) were also positively correlated with
Site Q1. None were correlated with site Q2.

3.6. Carbon accumulation rates in secondary forest

We calculated the accumulation rates also at three scales:
regional, landscape and local. To estimate the average accumulation rate at the regional level, we modeled C in total living biomass
against age with a ratio estimator (linear regression through origin of total living biomass of each plot against its age). The
forest fallow accumulates on average 3.60 0.41 Mg C ha1 yr1
(Fig. 3a). Young fallows (<25 years) accumulate C at a rate of
4.67 0.51 Mg C ha1 yr1 , whereas the rate of C accumulation in
old fallows (25 years) decreased to 3.00 0.66 Mg C ha1 yr1 . To
estimate the accumulation rate at the landscape level, we estimated the rates of C in total living biomass for each age class using
the estimated increase in C of living biomass of each plot (C in
TLB divided by age), the highest rates occur in the age class 15
year (7.30 3.24 Mg C ha1 yr1 ) and show a downward trend to
about 2.55 0.94 Mg C ha1 yr1 in the 3140 year age class (see
Fig. 3b).
The contribution of non-tree living biomass in the accumulation rates was only important in the rst age class, but as this
pool remains more or less constant over time, the contribution
to the biomass accumulation decreases as tree biomass increases.
The accumulation of dead biomass was very high in the rst age

Table 5
Average carbon content (Mg C ha1 ) in each age class of secondary forest.
Age class (N)
Living biomass
Above tree
Roots tree
Total tree (TreeB)
Non tree
Total (TLB)
Dead biomass
Dead woody debris
Litter
Total (TDB)
Dead and living biomass
(TLDB)
Soil organic carbon (SOC)
010 cm
1120 cm
2130 cm
030 cm
Total carbn (C)

15 (14)
(Mg C ha1 )

610 (15)
(Mg C ha1 )

1115 (13)
(Mg C ha1 )

1620 (5)
(Mg C ha1 )

2125 (6)
(Mg C ha1 )

2530 (5)
(Mg C ha1 )

3140 (5)
(Mg C ha1 )

20.1a
3.9a
24a
(21%)
1.0
25.0a
(22%)

36.8a
6.9a
43.7a
(31%)
0.9
44.6a
(31%)

57ab
10.2ab
67.2ab
(45%)
1.2
68.4ab
(45%)

52.4ab
9.5ab
61.8ab
(35%)
0.8
62.6ab
(35%)

79.1b
13.7b
92.8b
(47%)
0.9
93.7b
(47%)

89.6b
15.2b
104.9b
(50%)
0.6
105.4b
(50%)

82.1b
14.1b
96.2b
(52%)
1.0
97.2b
(52%)

1.1
7.8
8.9
(8%)
33.8a

3.3
7.6
10.9
(8%)
55.5a

4.4
8.1
12.6
(8%)
81.0ab

0.8
6.7
7.5
(4%)
70.1ab

5.7
6.8
12.5
(6%)
106.2b

6.5
6.4
12.9
(6%)
118.4b

6.7
7.2
13.9
(7%)
111.1b

(29%)

(39%)

(54%)

(39%)

(53%)

(56%)

(60%)

38.1
25.1
10.3
75.3
(65%)
115.4a

43.6
23.6
8.3
78.8
(55%)
142.8ab

38.5
14.9
6.0
62.6
(42%)
150.4ab

43.6
32.6
9.6
91.9
(52%)
178.1abc

44.7
24.1
9.2
82.4
(41%)
199.5abc

51.6
19.3
10.2
88.4
(42%)
211.5c

34.9
18.4
7.2
62.3
(33%)
186.1bc

Age classes were 15, 610, 1115, 1620, 2125, 2630, and 3140 years after abandonment. Between parenthesis the percentage of C in the pool in relation to total C.
Different exponents indicate signicant differences between age classes (p < 0.05; ANOVA). The average of soil organic carbon was derived from log-transformed average at
each depth class and total.

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D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

Table 6
Correlation coefcients of C pools and accumulation rates of secondary forests with independent variables.
Age
Pool or pool change
TreeB
TLB
TLDB
DWD
TDB
Total C
SOC010
SOC1120
SOC2130
TreeB Incr
TLB Incr.
TDB Incr
TLDB Incr
a
b

ra
0.63
0.64
0.65
0.32
0.24
0.51

0.55
0.56
0.63
0.64

LU-Intensity

Site Q1

Site Q2

pb

<0.01
<0.01
<0.01
<0.05
<0.1
<0.01

0.63
0.63
0.65
0.24
0.21
0.47

<0.01
<0.01
<0.01
<0.1
<0.1
<0.01

0.25
0.25
0.26

<0.05
<0.05
<0.05

0.23
0.41

<0.05
<0.01

0.20
0.19

<0.10
<0.10

0.20

<0.10

<0.01
<0.01
<0.01
<0.01

0.45
0.48
0.81
0.62

<0.01
<0.01
<0.01
<0.01

0.26

<0.05

0.49
0.48

<0.01
<0.01

r = Spearman correlation.
p = probability of error.

class, more than 3 Mg C ha1 yr1 , due to the large initial litter
pool. As the litter pool remained more or less constant after the
rst ve years and the dead woody debris pool was increasing
slowly, the contribution of dead biomass to the total dead and living
biomass accumulation rate decreases slowly until age class 1115
and remains more or less constant (about 0.5 Mg C ha1 yr1 ) from
age class 1620 years onward (Fig. 4).

Fig. 3. (A) Linear regression between carbon in living biomass and age. (B) Accumulation rates of carbon in living biomass in each age class.

3.7. Modeling carbon stocks and accumulation rates against age,

LU-Intensity and site quality
To model the accumulation rate at the local community level,
we tested if linear relations exist between the stocks and accumulation rates on the one hand and age, LU-intensity and the
site quality indices on the other hand. All multiple linear equations of carbon stocks that incorporate tree biomass (TreeB, TLB,
TLDB) as dependent variables include age (positive), LU-Intensity
(negative non-signicant; p < 0.05)) and Site Q1 (positive) as independent variables. It is interesting to note that multiple linear
equations of soil organic carbon (SOC) exclude fallow age as an
independent variable at any of the depth classes. The equations of
SOC for the three depth classes all contain Site Q2 as a positive
independent variable (p < 0.01), whereas the equation describing
SOC010 comprises additionally LU-intensity (negative p < 0.1) and
Site Q1 (positive, p < 0.05) and SOC2130 include Site Q1 (negative,
p < 0.01). Dead woody debris (DWD) and total dead biomass (TDB)
are positively correlated with age and include Site Q1 in the regression equation, whereas litter include Site Q1 positively and Site
Q2 negatively in the regression, although the latter not signicant
(Table 7).
The forward stepwise linear regression equations between the
accumulation rates (TreeB Incr, TLB Incr, TLDB Incr) as dependent
variables and age, LU-Intensity, Site Q1 and Q2 as independent variables, all include age (negative, varying p), site Q1 (positive, varying

Fig. 4. Accumulation rates of carbon in tree biomass, living biomass and living and
dead biomass in each age class.

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284
Table 7
Multiple linear regression between C pools and accumulation rates with independent variables.

TreeB
TLB
TLDB

LU-Intensity

Site Q1

Site Q2

(s.e.)

(s.e.)

(s.e.)

(s.e.)

2.18
(0.40)
2.19
(0.40)
2.35
(0.43)

9.70
(8.63)
9.39NS
(8.21)
9.20NS
(8.96)
NS

6.39*
(3.62)

1.63
(0.48)
1.66
(0.48)
2.08
(0.52)
0.45
(0.07)
0.06NS
(0.05)
0.15*
(0.06)
0.76**
(0.32)

2.07*
(1.21)

0.59
(0.21)
0.23
(0.08)
0.22
(0.08)
0.24**
(0.09)

Litter
DWD
TDB

0.17
(0.06)
0.42
(0.07)

SOC010
SOC1120
SOC2130
TreeB Incr
TLB Incr
TLDB Incr

0.10**
(0.04)
0.11
(0.04)
0.11*
(0.06)

Living biomass = 105 * (1 - exp(a * Age)) b

a = - 0.070 0.028, p < 0.01; b = 0.98 0.38, p < 0,05
r = 0.70; var. expl 48.8%

150

100

50

0.17NS
(0.13)

20

40

60

80

100

Age (Yr)

3.11
(0.61)
2.57
(0.15)
2.27
(0.36)
0.18NS
(0.14)
0.21NS
(0.14)
0.19NS
(0.15)

All equations and coefcients (C) have a probability of error of less than 1% (p < 0.01),
except where indicated. **p < 0.05; *p < 0.1; NS, non-signicant. In parenthesis
standard error of the coefcient. TreeB, Tree biomass; TLB, Total living biomass;
TLDB, total living and dead biomass; SOC, Soil organic carbon; Incr, annual accumulation rate.

p) and Site Q2 (positive, non-signicant) as independent variables,

while TLDB Incr also incorporates LU-Intensity as a positive variable
(p < 0.05; Table 7).
To estimate the time required for forest fallow to reach the carbon densities of undisturbed forests, we calculated an asymptotic
ChapmanRichards growth equation between age and total living
biomass, using the average carbon in living biomass of undisturbed
forest as the upper limit (105 14.6 Mg C ha1 ). This type of equation accounts for the progressive reduction over time in the biomass
accumulation rate (Zeide, 1989). Based on the outcome of this equation a rapid increase in living biomass can be observed in the rst
40 years, after which living biomass increases slowly stabilizing
between 60 and 85 years (Fig. 5). The recovering time of C in living
biomass is therefore estimated to lie be between 60 and 100 years,
taking into consideration also the uncertainty in the estimation of
living biomass in undisturbed forest (Table 5). To test the outcome
of the equation we derived the current annual increment of living
biomass from the growth equation, subsequently we calculated the
average increment of each age class based on the annual increment
estimation of the growth model and compared these with the mean
average living biomass increments in each age class derived from
the eld plot data (Fig. 3b). The model results coincide well with
the eld data for almost all age classes (Fig. 6).

Fig. 5. Total living biomass stock as a non-linear ChapmanRichard growth function

of age.

In accordance with current knowledge on succession dynamics, an initial rapid accumulation of living biomass occurred during
the rst succession stages, mainly due to rapid growth of early
successional species. The variation of carbon densities in the secondary vegetation show a direct relation with age, mainly due to
the increase in living tree biomass along the age gradient. All pool
combinations that include tree biomass show an increasing trend
in density according to age, although the shape of the trends may
differ. Also dead woody debris showed a positive relation with age
as a continuous variable, although the results should be treated
with caution. Soil organic carbon and litter did not show any linear
trend with age.
Carbon in tree biomass in undisturbed and disturbed forests in
our study site was higher than the average observed for the humid
tropics of Mexico (52 Mg C ha1 in all types of undisturbed tropical
forests and 19 Mg C ha1 in disturbed tropical forests; De Jong et al.,
2010) or Yucatn Peninsula, but lower than nearby regions in Chiapas or Veracruz (Table 8). Total living and dead biomass and total C
in mature and secondary forests were much higher in the Selva
Lacandona region (276.3 Mg C ha1 in TLDB and 452.6 Mg C ha1
in Total C for undisturbed forest and 136.4 Mg C ha1 in TLDB
and 272.3 Mg C ha1 Total C for secondary forests; De Jong et al.,
2000) and Los Tuxtlas, Veracruz (195.1 Mg C ha1 in TLDB and
391.6 Mg C ha1 in Total C; Hughes et al., 2000). However, Cairns
et al. (2000) found 59.9 Mg C ha1 and 119.3 Mg C ha1 in medium
and tall rain forest of Chiapas and Veracruz respectively. Both De
Jong et al. (2010) and Cairns et al. (2000) used data derived from

Mean annual increment in age class:

* Plot data

Mg C Ha-1 yr-1

Dependent variables

Age

Living biomass (Mg C ha-1)

Independent variables

200

79

Model average

4. Discussion
Current annual increment

The relationship between land use and forest succession is complex: the intensity of land use, the number of years the forest is
recovering and soil and site quality have been identied as strongly
inuential in the nature and rate of forest regrowth (Purata, 1986;
Hughes et al., 1999; Moran et al., 2000; Silver et al., 2004).

0
0

10

15

20

25

30

35

40

45

50

55

60

Age (yr)
Fig. 6. Current and mean annual growth of carbon in living biomass, estimated from
the ChapmanRichards non-linear growth function and plot data.

80

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

Table 8
Reported carbon stocks and accumulation rates of forests in Southern Mexico.
Author(s)

Region or state

Annual rainfall
(mm yr1 )

Living above-ground biomass

stock (Mg C ha1 )

Living above-ground carbon accumulation

rate (TLB Incr) (Mg C ha1 yr1 )

Cairns et al., 2000, old growth,

inventory-based
De Jong et al., 2010, old growth,
inventory-based
This study, old growth, selective
plots
Urquiza-Haas et al., 2007; Late
secondary (30 yr), selective plots
This study, late secondary (>25 yr),
selective plots
Hughes et al., 1999, secondary
forest, selective plots
This study, all secondary plots,
selective plots
De Jong et al., 2010, secondary
forest, inventory-based
Read and Lawrence, 2003, young
secondary, selective plots
This study, young secondary
(<25 yr), selective plots

Southern Mexico

>1500

51.3 3.4

NR

Humid tropics

>1500

52 3.6

NR

Chiapas

15002500

90.2 13.2

NR

Yucatn Peninsula

10001500

47.6 6.7

1.3 0.2*

Chiapas

15002500

86.7 23.2

2.6 0.7

Veracruz

>4000

67.1 30.9

3.4 1.1*

Chiapas

15002500

51.5 7.8

2.4 0.3*

Humid tropics

>1500

19 2.7

NR

Campeche

9001400

17.0 4.1

1.5 0.2*

Chiapas

15002500

43.4 7.1

3.0 0.7*

NR, not reported; all data refer to carbon in above-ground biomass. * Accumulation rates (a) derived from original data and applying formula: TLB (in Mg C ha1 ) = a* Age.
1 Mg biomass = 0.45 Mg C.

national forest inventory databases, which are based on a systematic grid of inventory plots, whereas this study and the studies of De
Jong et al. (2000) and Hughes et al. (2000) were based on selectively
established sample plots, according to predened characteristics. In
our case, the selection criterion was number of years after abandonment of cultivation, in the case of De Jong et al. (2000) the criteria
were either disturbed or undisturbed and Hughes et al. (2000)
selected undisturbed plots within a nature reserve. The lower estimates derived from systematically located plots compared to the
estimates derived from selective sampling coincides with Brown
et al. (1989) and Brown and Lugo (1992).
Our estimated average accumulation rate over the whole
age trajectory (3.60 0.41 mg C ha1 yr1 ) are higher than those
derived from Read and Lawrence (2003) and Urquiza-Haas
et al. (2007) for the southern Yucatan Peninsula (1.52 0.51
and 1.26 0.16 mg C ha1 yr1 respectively), but similar to
the rates reported by Hughes et al. (1999) for Veracruz
(3.44 1.09 Mg C ha1 yr1 ). According to Silver et al. (2000),
forests within different life zones accumulate biomass at approximately the same rate in the rst 20 years, but in the following
2080 years, moist forests (10002500 mm yr1 ) accumulate
biomass at a lower rate than wet forests (>2500 mm yr1 ). The
differences observed in the accumulation rates between our site
(15002500 mm yr1 ) and the somewhat dryer Yucatn Peninsula
(9001500 mm yr1 ) in the rst 25 years indicate that rainfall
below 1500 mm yr1 could be limiting biomass accumulation also
in earlier successional stages.
Turner et al. (2001) found that 25 years old forest fallows accumulated about 80% of biomass observed in mature forest. This is
similar to our results where carbon in living biomass of stands
aged 2125 years reached 89% of that of undisturbed forests. However, Lawrence and Foster (2002) and Urquiza-Haas et al. (2007),
reported that 25-year-old secondary forests contained between
38% and 40% of aboveground biomass of mature forests. Forest fallow plots of between 25 and 40 years in our study area presented
carbon densities similar to those observed in undisturbed forests.
However, estimating the recovery time with the ChapmanRichard
growth function it would take more than 60 years to reach carbon densities of undisturbed forest, which is similar to the range
of 5595 years of recovery time reported by Read and Lawrence
(2003) for the forest in the Yucatn Peninsula and the recovery

time of 73 years reported by Hughes et al. (1999) for a wet tropical

forest in Veracruz, or 80 years reported by Vargas et al. (2008) for
forest in the Yucatn Peninsula to recover biomass after burning,
applying a similar Richard growth function.
4.1. Factors inuencing carbon densities and carbon
accumulation
Age, LU-intensity and site quality together were directly correlated to tree biomass in secondary forests, with tree biomass
increasing along the age and site Q1 gradient and decreasing
along the LU-intensity gradient. Along a secondary forest chronosequence from 6 months to 50 years, Hughes et al. (1999) found that
pool sizes were positively correlated with forest age and negatively
with the duration of land use prior to abandonment. We did not
nd any correlation between the number of agricultural cycles and
biomass or biomass increments when considering the whole data
set. This is expected, as the number of cycles was always one in
the older age classes, making comparisons of biomass or biomass
increments between the different numbers of cycles difcult.
Of the three factors we analyzed, age was the most important, with increasing trend of carbon in the biomass pool but a
decreasing trend in the carbon accumulation rate along the age
gradient. Both site quality indices were positively correlated with
soil C in secondary forests and all pool combinations that include
the tree component in undisturbed forest. Total dead biomass was
highest in undisturbed forests and somewhat larger in sites used
once or twice compared to sites used three to four times, although
the variation within the number of cycles was too high to detect
signicant differences (Fig. 7).
Other studies found correlations of biomass stock and accumulation rates with length of cultivation period (Kauffman et al., 2009)
and number of cultivation cycles ((Eaton and Lawrence, 2009) in
secondary forests, whereas the whole cycle period (including fallow) is also considered important in terms of maintaining the
agricultural productivity (Nair, 1993). Ochoa-Gaona et al. (2007)
used an integrity index (combining cultivation period, number of
years in fallow and number of cultivation cycles) to explain loss of
biodiversity in secondary forests. Levy-Tacher and Aguirre (2005)
also proposed a land-use intensity index that combines the number and length of cultivation and fallow cycles, similar to our study.

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

Total dead biomass (Mg C ha-1)

25

20

15

10

Median and non-outlier range

1-2

3-4

Number of cycles
Fig. 7. Dead biomass stocks in relation to number of agricultural cycles.

Uhl et al. (1988) reported that secondary forests of sites that had
experienced relatively light intensities of land use had higher rates
of aboveground biomass accumulation than those with high LUintensity. In our case, the positive correlation between LU-intensity
and biomass accumulation rates, combined with the positive correlation between the index and Site Q2 generates the idea that
farmers may be able to select plots with higher quality for more
intensive slash-and-burn agriculture, where logically carbon in
biomass accumulates faster after abandonment, although we did
not test this hypothesis.
4.2. Soil
The transformation of forest land into agricultural land leads to
substantial losses of the above-ground biomass, but its effect on
soil C stocks remains poorly understood. It is commonly assumed
that after conversion to agricultural use the soil is impoverished
in C which is reversed during the fallow period (Greenland and
Nye, 1959; Raich, 1983; Cerri et al., 1991; Lugo and Brown, 1992).
In contrast with our expectations, soil C storage from 0 to 30 cm
in secondary forests did not increase with age or decrease due to
conversion to secondary forest. Within each depth class, secondary
forest soil C storage was roughly the same and did not show any
relationship with increased aboveground C storage. The mean SOC

81

storage of all fallow sites together was similar to SOC in primary

forest (74.9 t C ha1 in secondary plots, compared to 74.8 t C ha1
in the primary forest plots, Table 3) and there was no statistical
difference in total SOC or in SOC at any of the three depth classes.
Hughes et al. (1999) found that soil C pools (to 1 m depth) of
humid forests ranged from 139 to 249 Mg ha1 , and that patterns
of variation were not related to either forest age or duration of land
use, similar to our ndings. Based upon analysis of soil pools in
Amazonia, Hughes et al. (2002) and McGrath et al. (2001) concluded
that soil C (and nutrient) pools were most strongly and positively
correlated with clay content. Contrary to these ndings, our data
presented a negative correlation between C-content (in % of volume) and clay content at all three layers (r = 0.37 at 010 cm,
0.43 at 1120 cm, and 0.33 at 2130 cm; p < 0.01).
Silver et al. (2000) calculated soil C accumulation rates in regenerating tropical forests to range from 0.2 to 1.0 Mg C ha1 yr1 in
secondary forests. These rates are within the sampling errors of
most studies that examine C dynamics along chronosequences.
Marin-Spiotta et al. (2008) cautioned that bulk soil C measurements
are often too coarse to detect changes over forest successional time
periods, and may lead to the erroneous conclusion that soil C has
not responded to land-use change. A lack of soil C accumulation
with increased secondary forest age is not common in the tropics
(Rhoades et al., 2000; Silver et al., 2000; Feldpausch et al., 2004),
although it has been reported previously by Hughes et al. (1999)
in forests of Mexico. High spatial variation within and among sites
for reasons unrelated to site age can introduce errors (Yanai et al.,
2000; Yanai et al., 2003). Site factors such as aspect, slope, elevation, and soil type may locally inuence mineral soil C storage. The
number and diversity of factors that vary among sites within a
chronosequence highlight the need for more detailed time series
measurements within individual sites, as suggested by Chazdon
et al. (2007). Data are required that measure the effects of soil
characteristics (i.e., fertility, texture, chemistry) and prior land use
on rates of aboveground biomass and belowground C accumulation and would thus greatly improve our ability to predict soil-C
accumulation across landscapes and regions.

4.3. Scaling the results

All biomass stock and accumulation rates were correlated to age
and LU-Intensity, only with opposite signs. It therefore seems necessary to consider age and LU-Intensity as explaining factors of both
standing biomass and biomass accumulation rates at a landscape
level. This will result in signicant overall correlations, which can

Table 9
Carbon stock and accumulation rates applied at different scales.
Data type

Scale

Forest type
Stratication
Area

Medium-stature lowland rainforest

Secondary and old growth forest
Secondary medium-stature forest:
900,000 ha
Average stock, Average accumulation
rate (Table 4; Fig. 3a)

Regional-state

Models to be applied

Landscape

Local communities

Age classes
El Ocote: 50,000 ha

Age, LU-Intensity, Site Q1 and Q2

Community: 10002000 ha

Age class dependent stock and

accumulation rate (Table 5; Fig. 3b)

Regression models of stock and

accumulation rates against age,
LU-intensity and/or site quality
(Table 7; Fig. 5)
Age, LU-intensity, Site Q1 and Q2. Age
and LU-intensity from interviews and
validated with time series; Site Q1 data
from sample points in each
community, Site Q2 from visual
observations
Monte Carlo analysis approach.

Minimum data required and source

Total area of secondary forest, derived

from LU-maps or satellite imagery

Age distribution and LU-intensity of

secondary forests, derived from
time-series analysis of satellite
imagery

Uncertainty analysis due to data

requirements (IPCC, 2000)

95% CI of stock and accumulation rate

(linear regression between age and
total biomass)

Error propagation approach

82

D.E. Orihuela-Belmonte et al. / Agriculture, Ecosystems and Environment 171 (2013) 7284

be used successfully to estimate biomass parameters over larger

areas. However, if interest is vested in predicting biomass for particular sites, it may be more fruitful to use additional data collection
that account for specic site conditions or disturbance events. This
is indicated by the large variation observed in Fig. 3, which cannot be explained by a simple linear model. Through the alternative
methods we would obtain propositions in terms of probabilities
of nding certain values of biomass parameters for site parameters independent of age such as land use intensity, soil depth, site
quality, etc. A scale-dependent combination of forest type, landscape and site-specic models allows adapting local estimations
to landscape and forest type level estimations, while conserving
uncertainties in the estimations (Table 9).

5. Conclusions
REDD+ is a proposed performance-based mechanism under
negotiation through the United Nations Framework Convention
on Climate Change (UNFCCC), which will require demonstrated
emission reductions through improved forest conservation, sustainable forest management, and/or enhancement of carbon stocks.
They suggest that research should focus on how carbon sequestration varies with differing levels of community engagement and
autonomy, and across diverse tenure regimes and landscapes. A
key question in the debate concerns the level (scale) at which
accounting needs to be carried out and incentives offered for REDD+
activities. The scale for accounting of REDD+ has profound implications for the effectiveness, efciency and equity of the REDD+
mechanism (Angelsen et al., 2009). As activities will be implemented at a local scale, if performance-based nancial systems
will be developed for REDD+, the countries will need to be able
to up-scale estimations over time and space from local (community), through subnational landscapes to national accounting
systems.
One of the largest sources of uncertainty in GHG accounting
rests in the spatial variation of aboveground carbon stocks and
stock changes in primary forests, secondary forests and on fallow
land (Asner, 2011). In countries like Mexico land tenure is such
that REDD+ activities will be implemented at a local scale where
landowners will be invited to change their land-use strategies.
Particularly if the country implements performance-based stock
enhancement activities at this scale, factors that may affect carbon accumulation rates have to be taken into account. These in
turn need to be up-scaled to landscape and regional estimates with
cost-efcient methodologies.
As age of secondary vegetation is the main factor explaining
the variation in C-stock and accumulation rates independent of the
scale of analysis, this can be used as the basis to scale the estimations from community level, through landscapes up to forest type
(Table 9).
The information required at the community level would be the
age distribution of secondary vegetation and their LU-intensity
(which is correlated with environmental site characteristics of Site
Q1), and samples could be taken to estimate the variation in textural
and chemical characteristics of the soils, which in general is costly
due to laboratory procedures that are expensive. At the landscape
scale, the age class distribution and LU-intensity would be adequate to estimate the C-accumulation potential, these data can be
derived from time series analysis of satellite imagery (e.g. Hayes
and Sader, 2001; Yang and Lo, 2002; Lu et al., 2004). The total
area of secondary vegetation would be the source of information,
derived from land-use maps or satellite imagery, to estimate the
rate of C-accumulation in secondary forests within a forest type. As
data requirements and modeling complexity increases from region
to community, the uncertainty analysis required to estimate the

condence intervals of the results becomes more complex, from

simple 95% condence intervals of average biomass densities or
accumulation rates at the regional scale to complex Monte Carlo
simulations at the community scale (Table 9).
The secondary medium stature rainforest covers about
8.7 106 ha in Mexico. Of these, an estimated 900,000 ha are
located within the 15002500 rainfall zone, with an estimated
potential C-accumulation rate of 3.60 0.41 Mg C ha1 yr1 (this
study) and 7.8 106 ha are located within the 9001500 mm
rainfall zone, with an estimated C-accumulation potential of
1.52 0.24 Mg C ha1 yr1 (Read and Lawrence, 2003). If these
areas were to be managed as part of the REDD+ stock enhancement activity, the C-accumulation potential of the whole secondary
forests is estimated at 56.7 8.4 Tg CO2 yr1 , which is equivalent to
more than 65% of the net annual emissions between 1993 and 2002
of the whole LULUCF sector of Mexico (De Jong et al., 2010). Secondary forest is considered by farmers as temporal land reserves
that can rapidly and readily be converted to other land uses as
a response to demands of certain products or services (e.g. bioenergy, GHG mitigation, food, timber). As such, management of
these forests for GHG mitigation may be regarded as a key strategy
for Mexican REDD+ policy.

Acknowledgements
We gratefully thank two anonymous reviewers for their valuable comments, which improved the paper substantially. All the
institutions and persons who helped carry out this study, in particular Ing. Roberto Escalante and MC Karla Leal of Conanp, Biol.
Froiln Esquinca Cano of SEMAHN, Dr. Cristian Tovilla Hernndez of ECOSUR-Tapachula. Financial assistance was obtained from
CONACyT through a scholarship for DEOB. Financial assistance of
USAID/ABT through Ambio facilitated the eldwork, for which we
are very grateful. Additional funding was obtained from CONAFOR
for complementary eldwork and laboratory analysis. We are particularly grateful to all the people of the communities Armando
Zebada, Nuevo San Juan Chamula, Tierra Nueva, Veinte Casas,
Emiliano Zapata, Emilio Rabasa and Encajonado to allow us to work
in their plots, to live in their houses and to assist with the eldwork, in particular Manuel Ruz, Manuel Daz, Javier Hernndez,
Eduardo Hernndez, Jos Antonio Gmez, Sal Argueta and David
Hernndez, and nally we thank Margeli Nuril Acero and Diana L.
Rodrguez O. for their help in the laboratory.

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