tr
u
aw
ngap
Pana
Was
on, N
a r t i c l e i n f o
Article history:
Received 2 August 2012
Received in revised form 27 January 2013
Accepted 7 February 2013
a b s t r a c t
Carbon is stored in forests predominantly in live biomass and in
soils, with smaller amounts in coarse woody debris (Malhi et al.,
2009; Sierra et al., 2007). In tropical forests worldwide, about
50% of the total carbon is stored in aboveground biomass and
soil, while a secondary forest in the Philippines contained 50%
more carbon aboveground than in soil (Lasco et al., 2004).
The differences in carbon storage among tropical forests reflect
variation in a number of factors, including tree community compo-
sition, disturbance history, successional stage, climate, and soil fer-
tility. Secondary forests are of particular significance, given that the
proportion of tropical forests that are secondary is projected to con-
tinue to increase due to increasing anthropogenic pressure and the
movement of populations towards urban centers (Thomlinson
et al., 1996; Wright, 2005). Thus, carbon stocks and uptake in sec-
ondary forests are an increasingly important part of global tropical
⇑ Corresponding author at: Center for Tropical Forest Science, National Institute
of Education, 1 Nanyang Walk, Singapore 637616, Singapore. Tel.: +65 6790 3825;
fax: +65 6896 9414.
E-mail address: ngokangmin@gmail.com (K.M. Ngo).
1 Present address: Finnish Forest Research Institute, Jokiniemenkuja 1, PO Box 18,
Forest Ecology and Management 296 (2013) 81–89
Contents lists available at
Forest Ecology an
journal homepage: www.elFI-01301 Vantaa, Finland.1. Introduction
Tropical forests play an important role in the global carbon cy-
cle. They contain about 40% of global terrestrial carbon, account for
more than half of global gross primary productivity, and sequester
large amounts of CO2 from the atmosphere (Beer et al., 2010;
Grace, 2004; Pan et al., 2011). Slightly more than half of the carbon
in tropical forests is in the neotropics, with the remainder in Asian
and African forests (Dixon et al., 1994).
50% is stored in the top 1 m of the soil (Dixon et al., 1994). How-
ever, there are marked differences among sites. For example, an
African moist tropical forest had more than three times as much
carbon in aboveground biomass as in soil to 1 m depth (Djomo
et al., 2011), while a Peruvian montane forest had twice as much
carbon in soil as in aboveground biomass (Gibbon et al., 2010). In
Asia, a tropical seasonal forest in China (Lü et al., 2010) and a selec-
tively-logged lowland dipterocarp forest in Sabah, Malaysia (Saner
et al., 2012), both contained twice as much carbon in biomass as inKeywords:
Aboveground and belowground biomass
Carbon pools
Coastal hill dipterocarp forest
Ecosystem carbon
Necromass
Tropical rain forest0378-1127/$ - see front matter  2013 Elsevier B.V. A
http://dx.doi.org/10.1016/j.foreco.2013.02.004Tropical forests contain large reserves of carbon that are vulnerable to perturbation linked to human
activities, including deforestation and climate change. Accurate estimates of forest carbon are therefore
required urgently to support efforts to conserve tropical forests. We quantified carbon stocks in primary
and 60-year-old secondary forest plots located on infertile Ultisols in Bukit Timah Nature Reserve, one of
the few remaining areas of forest in Singapore. We used tree census data for 24.2 ha of primary forest and
23 ha of secondary forest, together with allometric equations, to estimate aboveground and coarse root
biomass. Coarse woody debris stocks were censused along 2.44 km and 2.12 km of transects in primary
and secondary forest, respectively. Soil carbon and fine root carbon stocks were assessed from soil sam-
ples taken to 3 m depth in a 2-ha secondary forest plot and a 2-ha primary forest plot, combined with
bulk density measured in a nearby soil profile pit. Total estimated carbon stock in the primary forest,
which was located on the hilltop and upper slopes (80–115 m elevation), was 337 Mg C ha1, of which
50% was aboveground biomass, 33% in soil, 12% in coarse roots, 4.6% in coarse woody debris, and 0.8%
in fine roots. In the secondary forest, located on lower slopes and valley (50–85 m elevation), the total
carbon stock was 274 Mg C ha1 and the relative importance of aboveground biomass and soil were
reversed, with 38% in aboveground biomass, 52% in soil, 6.9% in coarse roots, 1.5% in coarse woody debris,
and 1.3% in fine roots. Including carbon in deep subsoil (i.e. to 3 m) increased soil carbon stocks by 40%
compared to 1 m depth. Overall, the 60-year-old secondary forest contained 60% as much biomass as the
primary forest, while the primary forest had lower carbon stocks than other primary forests in the region.
 2013 Elsevier B.V. All rights reserved.Carbon stocks in primary and secondary
Kang Min Ngo a,d,⇑, Benjamin L. Turner b, Helene C. M
Markku Larjavaara b,1, Nik Faizu bin Nik Hassan a, Sh
aCenter for Tropical Forest Science, National Institute of Education, 1 Nanyang Walk, Si
b Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Balboa, Ancon,
c SIGEO–CTFS, Smithsonian Institution, Department of Botany, MRC-166, PO Box 37012,
dNatural Sciences and Science Education Academic Group, National Institute of Educatill rights reserved.opical forests in Singapore
ller-Landau b, Stuart J. Davies c,
n Lumd
ore 637616, Singapore
ma
hington, DC 20013, USA
anyang Technological University, 1 Nanyang Walk, Singapore 637616, Singapore
SciVerse ScienceDirect
d Management
sevier .com/locate / foreco
tected forest on the island of Singapore. The site supports
months receiving more than 100 mm on average (National Envi-
nd Mronment Agency, 2012). Soils in BTNR are Typic Paleudults of the
Rengam series formed on Bukit Timah Granite (Ives, 1977),
although this differs from the classification of a pedon adjacent
to the primary forest plot studied here (see below). The soils are
very acidic and infertile (Burslem et al., 1994; Grubb et al., 1994),
with a particularly strong response of tree seedlings to phosphorus
addition (Burslem et al., 1994).
2.2. Field data collection
Data from three different censuses were used to estimate tree
biomass: 2008 censuses of all trees P1 cm dbh in a 2-ha primary
forest plot (LaFrankie et al., 2005) and in 1.74 ha of a 2-ha second-
ary forest plot (the excluded area includes some primary forest),
and a 2005 ‘‘Big Tree’’ survey that measured trees P30 cm dbh in
the whole 164-ha reserve (Fig. 1). Trees were tagged, mapped
and identified to species. Trunk diameters were measured at
1.3 m or above buttresses, and are henceforth referred to as dbh
(diameter at breast height), even if measurement height was not
at 1.3 m. Within the ‘‘Big Tree’’ survey, a 22.2-ha area of primary
forest and a 23-ha area of secondary forest were chosen for analy-dipterocarp forest growing on infertile soils developed on granite
bedrock (Burslem et al., 1994). We estimate carbon stored in living
trees, coarse woody debris, and soil. Importantly, we estimated soil
carbon to 3 m depth; most studies only sample to 1 m, but tropical
forest soils, including those at Bukit Timah, can be very deep (e.g.
>5 m in Bukit Timah; see Supplementary material) and previous
studies may therefore have underestimated soil carbon stocks.
2. Methods
2.1. Study site
Bukit Timah Nature Reserve (BTNR) is a 164-ha forest reserve in
central Singapore that contains the island’s largest remaining patch
of primary forest (LaFrankie et al., 2005). The reserve is naturally
dominated by coastal hill dipterocarp forest and contains Singa-
pore’s highest natural point (164 m above sea level). The core area
of BTNR is a 70-ha block of mainly primary forest dominated by
Shorea curtisii Dyer ex King, a hill forest species usually found at
higher elevation in Peninsular Malaysia (Symington et al., 2004).
The remainder of the reserve includes secondary forest regrowth
on agricultural land abandoned since the 1950s (Lau and Noor,
pers. comm.) and former cattle pasture dominated by the exotic
African tulip tree (Spathodea campanulata).
Climate is aseasonal, with an average temperature of 27.0 C be-
tween 1929 and 2011. Mean annual rainfall is 2342 mm with allforest carbon budgets. As more forests come under threat from
deforestation and degradation, additional information on carbon
stocks and pools in tropical forests worldwide is required to under-
stand controls on carbon stocks and cycling, to calibrate global car-
bon cycle models, and to support regulatory frameworks such as
the United Nations REDD program (Reducing Emissions fromDefor-
estation and Forest Degradation in Developing Countries).
In Singapore, more than 95% of the original forest has been
cleared, most of it prior to the 1870s (Corlett, 1992). Much of the
remaining forest cover is secondary, although a few small patches
of protected primary forest remain. Here we report carbon stocks
in long-term forest dynamics plots in primary and secondary for-
ests in Bukit Timah Nature Reserve, one of the few areas of pro-
82 K.M. Ngo et al. / Forest Ecology asis based on an analysis of species composition (unpublished data).
Coarse woody debris (CWD) was censused between September
2009 and February 2010, largely following the protocolsestablished by Larjavaara and Muller-Landau (2009a, 2009b,
2010, 2011). The CWD census was done along transects using
line-intersect methods (Warren and Olsen, 1964), with a little over
half the sampling effort concentrated in the 2-ha plots. Nine
40  40 m subplots from the 2-ha primary forest plot and seven
from the 2-ha secondary forest plot were sampled, with 160 m of
transects within each subplot (Larjavaara and Muller-Landau,
2009a). Ten 200 m transects were spread out regularly in the wider
reserve for sampling (Larjavaara and Muller-Landau, 2009b), five in
primary and five in secondary forest. Standing woody debris
P20 cm dbh was censused in the 2-ha plots only, and necromass
of individual stems was estimated from diameter using the equa-
tions above. Where stumps were shorter than dbh, diameter was
measured at the midpoint of the stump (Larjavaara and Muller-
Landau, 2009a). Because destructive sampling was not allowed in
BTNR, woody debris wood density was estimated from penetrom-
eter penetration using a relationship fitted for data from Barro Col-
orado Island, Panama (Larjavaara and Muller-Landau, 2010).
Soils were sampled between April and June 2008 in the 2-ha
plots only. Cores were taken systematically from alternate
20  20 m quadrats, giving a total of 26 sample locations in each
2 ha plot. In each plot, we used a 6 cm diameter constant volume
corer to take samples from 0 to 10 cm (26 cores per plot) and
10–20 cm (18 cores per plot) and then a 7.5 cm diameter auger
to take samples from 20 to 50 cm and 50 to 100 cm (10 cores for
each depth) and 100–300 cm (2 cores taken in 50 cm increments).
Samples were air-dried and roots and stones were removed by
hand. Fine roots (<2 mm diameter) were separated by hand, dried
at 60 C, and weighed. The soils were then sieved (<2 mm) and a
subsample ground for analysis. Soil carbon concentration was
determined by combustion and gas chromatography using a Ther-
mo Flash EA 1112 Elemental Analyzer (CE Elantech, Lakewood, NJ).
Bulk density was determined for surface soils (0–10 cm and 10–
20 cm) using a constant volume corer as described above (i.e., a
bulk density value was calculated for every sample). Total sample
weight was measured and corrected for oven-dried weight of fine
earth by determining moisture content on a subsample (105 C,
24 h) and correcting for root biomass (>2 mm). Bulk density was
determined for deeper samples (>50 cm) by digging a 2 m deep soil
profile pit close to the primary forest plot and taking bulk density
samples by the compliant cavity method every 10 cm. Information
on the profile, including profile description and analytical data, is
presented in Supplementary material.
2.3. Calculations
Aboveground biomass (AGB) of each tree stem was estimated
using the allometric equation for moist tropical forest from Chave
et al. (2005):
AGB ¼ q expð1:499þ 2:148 lnðdbhÞ þ 0:207ðlnðdbhÞÞ2
 0:0281ðlnðdbhÞÞ3Þ
where q is wood specific gravity, dbh is in cm, and AGB is in kg dry
mass. The generic moist tropical forest equation was used because
site-specific equations were not available, and because the annual
precipitation of BTNR falls within the interval 1500–3500 mm.
Aboveground biomass was calculated for trees of 1–30 cm dbh in
the 2-ha plots, and for the P30 cm dbh size class from the 2-ha
plots and the Big Tree survey. Data from the 2008 census for the
2-ha plots were used in this analysis. Each species was assigned a
wood specific gravity value obtained from a worldwide database
(Chave et al., 2005), with species level values used for 274 species,
anagement 296 (2013) 81–89genus level for 200 species and family level for 21 species. Below-
ground biomass in coarse roots was estimated using allometric
equations developed in Malaysia. The equation to estimate coarse
nd MK.M. Ngo et al. / Forest Ecology aroot biomass from dbh was taken from Niiyama et al. (2010) for pri-
mary forest (R2 = 0.98) and Kenzo et al. (2009) for secondary forest
(R2 = 0.94). We calculated confidence intervals for both AGB and
coarse root biomass using 1000 bootstraps over 20  20 m quad-
rats, thus providing information on uncertainty related to spatial
variation in biomass within the study area.
Woody debris volume per areawas calculated from transect data
using V ¼ p28L
P
d2i , where V is the volume per area (m
3/m2), L is the
total lengthof the transect (m) andd thediameter (m)of the ithpiece
ofwoodydebris encountered. Totalmass ofwoodydebriswas calcu-
lated using M ¼ p2L
P
ci where M is total mass per area (kg m2), L is
total transect length and c is cross-section mass (kg m1), i.e., dry
mass per unit length of the fallen log (Larjavaara andMuller-Landau,
2011). Mean woody debris values were calculated by treating 20 m
sections of all transects as replicates. Confidence intervals were cal-
culated by 1000 bootstraps over 20 m sections.
Soil carbon and fine root biomass per unit volume, and per unit
ground area, were calculated for each sample using bulk density
values.
To convert aboveground biomass, coarse root, fine root, and
coarse woody debris dry mass values to carbon stocks, we assumed
that 50% of the dry mass was carbon. Studies at nearby sites in
Malaysia having similar species composition have found average
carbon content close to 50% (Kenzo et al., 2010; Kenzo, pers. comm.).
3. Results
3.1. Aboveground biomass
There was significantly higher AGB in the primary forest than in
the secondary forest (Table 1). TreesP30 cmdbh contained 77% and
55% of the AGB in the primary and secondary forests, respectively.
Fig. 1. Map of the Bukit Timah Nature Reserve, Singapore, showanagement 296 (2013) 81–89 83Therewas significantly higher AGB in the 1–10 cm andP30 cm dbh
size classes in the primary forest, while the secondary forest had sig-
nificantly higher AGB in the 10–30 cm size class.
The 10 species contributing the most biomass in the P30 cm
size class accounted for about half of the total AGB in the primary
forest, but only 28.7% in the secondary forest (Supplementary
material Table 1). In contrast, the ten species contributing the most
biomass in the 10–30 cm size class accounted for only 7.6% of the
total AGB in the primary forest, but 31.7% in the secondary forest
(Supplementary material Table 2). Dipterocarpaceae, the dominant
tree family, contributed a large proportion of AGB in the primary
forest. S. curtisii and Dipterocarpus caudatus made up 24% and
7.1% of AGB in theP30 cm size class (Supplementary material Ta-
ble 1). For the 10–30 cm size class, S. curtisii again accounted for
the highest percentage of AGB, followed by Streblus elongatus (Mor-
aceae) and Timonius wallichianus (Rubiaceae) (Supplementary
material Table 2), both of which are common species in primary
and mature secondary forest. In secondary forest, Ixonanthes retic-
ulata (Ixonanthaceae) had the highest AGB in the P30 cm size
class, followed by Campnosperma auriculata (Anacardiaceae) (Sup-
plementary material Table 1), even though there were far more C.
auriculata individuals (288) than I. reticulata individuals (119).
3.2. Fine and coarse root biomass
The majority of the fine roots in both primary and secondary
forest plots were contained in the upper 10 cm of soil; the second-
ary forest contained more fine roots in this horizon than the pri-
mary forest (Table 3). No roots were detected in secondary forest
soils below 50 cm, while roots were detected to 3 m depth in the
primary forest plot. However, in the upper meter of soil the total
fine root biomass was 50% greater in the secondary compared
ing the locations of the primary and secondary forest plots.
compared to the secondary forest, although confidence intervals
throughout the profile) and most of the cation exchange capacity
Bulk density for the 0–10 cm depth was 0.79 ± 0.17 g cm
(mean and standard deviation of 26 samples) for the primary plot
Table 1
Tree aboveground biomass (AGB) and density in primary and secondary forests. Figures in parentheses indicate 95% confidence intervals based on 1000 bootstrap samples over
20  20 m subplots.
Tree size class (dbh) Primary forest Secondary forest
AGB (Mg ha1) Individuals (ha1) AGB (Mg ha1) Individuals (ha1)
1–10 cm 15.37 (14.40–16.34) 5909 (5547–6245) 11.53 (10.42–12.61) 1365 (1133–1614)
10–30 cm 60.96 (53.42–68.93) 336 (305–368) 81.85 (73.57–91.47) 468 (420–522)
a –83)
for
84 K.M. Ngo et al. / Forest Ecology and Management 296 (2013) 81–89was aluminum. Total phosphorus was also low (<10 mg P kg1 in
subsoil >50 cm deep) and the soils were extremely acidic through-
out (pH in deionized water6 4.0 in the upper meter). Below the
kandic horizon the soil contained 20% fine gravel, consisting of
angular quartz fragments from the granite parent material. A full
profile description and analytical information is provided in Sup-
plementary material.for the latter were wide and the difference was not statistically sig-
nificant. This may be due to the small sample size for standing
dead wood.
3.4. Soil carbon stocks
The soil profile pit excavated close to the primary forest plot
confirmed the soils as Ultisols (Typic Kanhapludult), with clear clay
accumulation in the subsoil and a low effective cation exchange
capacity (<5 cmolc kg1) in the clay enriched horizon (i.e., a kandic
horizon) (Soil Survey Staff, 1999). The soil contained very low con-
centrations of base cations (total exchangeable bases <1 cmolc kg1to the primary forest plot (Table 3). When roots to 3 m depth were
considered, the secondary forest contained only around one third
more fine root biomass than the primary forest.
Using the equations of Niiyama et al. (2010) and Kenzo et al.
(2009), we estimated that coarse roots (i.e., total belowground car-
bon minus fine root carbon) contributed 40.2 and 18.8 Mg C ha1
biomass in the primary and secondary forests, respectively.
3.3. Coarse woody debris
There was three times more necromass in the primary forest
(31.2 Mg ha1) than in the secondary forest (8.3 Mg ha1) (Table 2).
The majority of the necromass in both forests was standing woody
debris, which accounted for 61% and 71% of necromass in the pri-
mary and secondary forests, respectively (Table 2). There was con-
siderably more fallen and standing woody debris in the primary
P30 cm 258.66 (241.39–277.67) 79 (75
Total 334.98 (315.60–354.37)
a Stocks for trees P30 cm were averaged over the entire study area, while stocksCarbon concentrations in surface soil (0–10 cm) of the primary
plot (2.9 ± 0.8%, mean ± standard deviation of 26 samples) were
lower than in the secondary plot (4.1 ± 1.4%) (Fig. 2). This was re-
flected in differences in bulk density (see below), which was great-
er for the primary plot. Subsoil horizons in the two plots contained
Table 2
Coarse woody debris stocks in primary and secondary forests in Bukit Timah Nature Reser
bootstrap samples of 20-m transect sections.
Primary forest
Necromass (Mg ha1) Volume (m3 ha1)
Fallen 12.31 (8.40–19.37) 47.20 (35.18–77.4
Standing 18.87 (5.84–23.49) 58.07 (18.10–74.8
Total 31.18 105.27and 0.71 ± 0.24 g cm3 for the secondary plot. These values were
comparable to the value for 0–10 cm depth obtained by the com-
pliant cavity method in a soil profile pit adjacent to the primary
forest plot (i.e., bulk density = 0.89 g cm3). For the 10–20 cm
depth, bulk density was 0.97 ± 0.18 g cm3 for the primary plot
and 1.12 ± 0.28 g cm3for the secondary forest plot (n = 18 sam-
ples), compared to 1.36 g cm3 in the profile pit. Bulk density mea-
surements in deeper soils taken by the compliant cavity method in
the profile pit in the primary forest plot ranged between 0.97 and
1.31 g cm3, the variation reflecting the relatively large content of
coarse fragments in subsoil horizons (see above).
When converted to carbon stocks, more soil carbon was con-
tained in the secondary forest compared to the primary forest. In
the upper 1 m, for example, the primary forest contained
77.5 Mg C ha1 while the secondary forest contained
103.9 Mg C ha1, approximately one third more carbon (Table 3).
Including soil to 3 m increased carbon stocks to 110.8 and
143.2 Mg C ha1 for the primary and secondary forests, respec-
tively, an increase of 43% and 38%, respectively, compared to the
upper 1 m (Table 3).
3.5. Total carbon stocks in Bukit Timah Nature Reserve
The total carbon stock was greater in primary forest
(337 Mg C ha1) than secondary forest (274 Mg C ha1) (Table 4).
The secondary forest therefore contained 63 Mg C ha1 less carbon
than the primary forest, a difference of 19%.
Of the four main compartments measured, the majority of thesimilar carbon concentrations, with <0.5% in soils deeper than
50 cm, and <0.2% in soils deeper than 150 cm (Fig. 2). There was lit-
tle further variation down to >5 m, as revealed by measurements in
a soil profile pit adjacent to the primary forest plot (Supplementary
material). Soil carbon to nitrogen ratios were in general much
higher in the upper 50 cm of soil in the secondary forest (soil
C:N 22–31) compared to the primary forest (soil C:N 11–17).
3
115.66 (105.43–126.17) 60 (56–64)
209.04 (195.80–223.04)
trees <30 cm were based only on the 2-ha plots.carbon in both primary and secondary forests was contained with-
in aboveground biomass and soil (Table 4). However, there was
marked variation in the proportional contribution of these two
main pools between the two forests. The majority of the carbon
in primary forest was in aboveground biomass (49.8%), with only
ve, Singapore. Values in parentheses indicate 95% confidence intervals based on 1000
Secondary forest
Necromass (Mg ha1) Volume (m3 ha1)
7) 2.43 (0.61–5.09) 7.55 1.99–16.52)
6) 5.88 (0.96–13.81) 16.64 (2.95–37.63)
8.31 24.19
nd MK.M. Ngo et al. / Forest Ecology a32.9% in soil. In contrast, the majority of the carbon in the second-
ary forest was in soil (52.2%), with only 38.1% contained in above-
ground biomass (Table 4).
are thus confounded with forest age in our analyses. However,
Table 3
Soil carbon stocks and fine root biomass in primary and secondary forests in Bukit Timah
Depth (cm) Primary forest
Soil C (Mg C ha1) Fine roots (Mg h
0–10 22.1 (± 0.8) 2.72 (± 0.31)
10–20 12.2 (± 0.9) 0.60 (± 0.10)
20–50 19.4 (± 0.7) 0.81 (± 0.23)
50–100 23.8 (± 0.8) 0.57 (± 0.50)
100–150 13.4 (± 0.6) 0.48 (± 0.04)
150–200 8.3 (± 1.0) 0.03 (± 0.03)
200–250 6.8 (± 0.4) 0
250–300 4.9a 0.09a
Total to 1 m 77.5 4.70
Total to 2 m 99.2 5.20
Total to 3 m 110.8 5.29
a Only a single sample collected at this depth.
Soil carbon (%)
0 1 2 3 4 5
D
ep
th
 (c
m
)
0
100
200
300
400
500
Profile pit (primary forest)
Primary forest plot
Secondary forest plot
Fig. 2. Soil carbon concentrations in primary and secondary forest plots (to 300 cm
depth) and a profile pit (sampled to >500 cm depth) in Bukit Timah Nature Reserve,
Singapore. Error bars indicate standard errors.
Table 4
Carbon stock estimates for primary and secondary forests in Bukit Timah Nature
Reserve, Singapore. Biomass was assumed to contain 50% carbon.
Component Primary forest Secondary forest
Mg C ha1 % of total Mg C ha1 % of total
Aboveground biomass 167.5 49.8 104.5 38.1
Coarse roots 40.2 11.9 18.8 6.9
Fine roots 2.6 0.8 3.5 1.3
Soil (to 3 m) 110.8 32.9 143.2 52.2
Coarse woody debris 15.6 4.6 4.2 1.5
Total 336.7 100.0 274.2 100.0our study plots are reasonably representative of primary and sec-
ondary forests in the BTNR in general, and indeed, they encompass
a full 29% of the total forest area in the BTNR.
The much greater aboveground biomass in the primary forest
compared to the secondary forest was due in large part to a differ-
ence in the number of large trees. The top 10 species P30 cm dbh
made up 46.3% of total aboveground biomass in the primary forest.
In contrast, trees 10–30 cm dbh in the primary forest contained farOf the remaining pools, coarse woody debris was of much great-
er quantitative importance in the primary forest (4.6% of total car-
bon) compared to the secondary forest (1.5%), while the opposite
was true for fine roots (Table 4), although the latter made only a
small contribution to total carbon stocks (1%). The contribution
of coarse roots was greater in primary forest (11.9%) compared to
secondary forest (6.9%).
4. Discussion
The majority of the carbon in our study area at BTNR was stored
in aboveground biomass and soil. The contribution of these pools
to the total carbon stocks varied markedly between the primary
and secondary forests. Specifically, in primary forest the dominant
pool was aboveground biomass (50% of carbon) and soil made a
smaller contribution (33%), while the opposite was true in the sec-
ondary forest. It is important to note that our primary forest area is
largely on hill or ridge top, while our secondary forest area is on
lower slopes and valleys, and that these topographic differences
Nature Reserve, Singapore. Values in parentheses indicate standard errors.
Secondary forest
a1) Soil C (Mg C ha1) Fine roots (Mg ha1)
28.4 (± 2.4) 5.07 (± 0.50)
19.4 (± 1.9) 1.33 (± 0.24)
26.7 (± 2.7) 0.64 (± 0.15)
29.4 (± 6.8) 0
15.2 (± 1.8) 0
8.6 (± 1.1) 0
6.7 (± 0.6) 0
8.8 (± 0.2) 0
103.9 7.04
127.7 7.04
143.2 7.04
anagement 296 (2013) 81–89 85less biomass than in secondary forest, both in absolute and propor-
tional terms (18% vs. 39% of total aboveground biomass; 15.7 m2 vs.
17.0 m2basal area). This is closely related to the species composition
of the secondary forest, because most of the canopy species in the
secondary forest are pioneers that rarely grow beyond 30 cm dbh.
Primary forest aboveground biomass at our study site in BTNR is
comparable to most forests in the neotropics, while relatively low
compared to other sites in tropical Asia (Fig. 3). In general, neotrop-
ical primary forests contain less aboveground biomass than Asian
and African primary forests (Fig. 3). The canopies of Asian forests
are dominated by members of the Dipterocarpaceae, with signifi-
cant contributions from the Fabaceae. Both families are usually
wind dispersed (Ng and Whitmore, 1989; Symington et al.,
2004), which might have pre-disposed them to grow taller for
more effective dispersal of their seeds instead of widening their
crowns (Slik et al., 2010). The 60-year-old secondary forest had
AGB stocks 63% as large as those of the primary forest. This value
is consistent with rates of successional biomass accumulation
seen in other secondary tropical forests (Brown and Lugo, 1990;
Mascaro et al., 2012).
The confidence intervals on woody debris stocks in primary for-
est at BTNR overlap the range of those previously observed in the
region (Table 5). The mean estimates for BTNR suggest that this
site has relatively low stocks of fallen coarse woody debris, and rel-
atively high stocks in standing woody debris. However, confidence
intervals are high, especially for standing stocks. Further, differ-
ences in sampling methods may lead to discrepancies in total woo-
dy debris, because plot-based methods tend to produce lower
values than those measured by the line-intersect method (e.g.,
Chao et al., 2008). Nonetheless, we speculate that the apparent
abundance of standing dead trees at BTNR may be caused by light-
ning strikes, due to the higher elevation of the 2-ha primary forest
plot.
Soil carbon to 3 m depth in primary forest at BTNR constituted
around one third of the total carbon stock, and more than half the
carbon stock in the secondary forest. Soils are typically only as-
sessed to 1 m depth (e.g., Dixon et al., 1994) and the IPCC recom-
mendation is to sample to a minimum of 0.3 m (IPCC, 2006).
Accounting for soil carbon to 3 m depth in the BTNR plot increased
the soil carbon pool by approximately 40% relative to 1 m depth,
albeit our estimates of deep carbon have considerable uncertainty
as they are based on only two sample points per forest plot. Deep
soil carbon can be unstable (Fontaine et al., 2007) and might there-
fore be susceptible to climate-induced perturbation, particularly if
increasing tropical forest productivity promotes allocation of car-
bon below-ground, as appears to be the case in temperate forests
(e.g., Alberton et al., 2005). It is therefore important to include sub-
soil carbon in assessments of carbon stocks in tropical forests. Con-
sidering just the top 1 m of soil, soil carbon in primary forest at
BTNR appears to be within the range of other primary forests
(Fig. 4). Neotropical forests in general appear to have a higher pro-
portion of their carbon in soil than in aboveground biomass (Malhi
et al., 2009; Sierra et al., 2007), although additional studies are re-
quired to confirm this pattern.
We found higher soil carbon in the secondary forest than in pri-
mary forests, contrary to the dominant pattern reported in the lit-
erature (de Camargo et al., 1999; Sierra et al., 2007). Powers et al.
(2011) showed that soil carbon stocks may increase or decrease
Asia
AGB (Mg ha−1)
N
o.
 p
lo
ts
0080060040020
0
5
10
15
Chave et al. 2008
 Slik et al. 2010
BTNR
Africa
AG
N
o.
 p
lo
ts
5
10
15 Lewis et al. 2009
Ne
AG
86 K.M. Ngo et al. / Forest Ecology and Management 296 (2013) 81–890020
0
N
o.
 p
lo
ts
0020
0
20
40
60Fig. 3. Aboveground biomass of tropical forests in Asia, Africa, and the neotropics. The ar
each graph. (See above-mentioned references for further information.)B (Mg ha−1)
008006004
otropics
B (Mg ha−1)
008006004
Chave et al. 2008
 Malhi et al. 2006row represents the Bukit Timah Nature Reserve. Data are from the references beside
Valu
Volume (m3 ha1)
31.2 47.2 (35.18–77.47) 58.1 (18.10–74.86) 105.3
49.0
55.0
26.4
66.0 37.7 103.7
105.0 46.1 151.1
70.6 25.8 96.4
20.3
6.1
49.0
La Selva, Costa Ricah 46.3 6.5 52.8
33.3
23.2
nd Mafter land use conversion depending on soil type and precipitation.
Moist forest, Venezuelai 18.5 14.8
Madre de Dios, Peruj 19.0m 4.2
a Yoneda et al. (1977).
b Yoneda et al. (1990)’.
c Saner et al. (2012).
d Gale (2000).
e Chao et al. (2008).
f Sierra et al. (2007).
g Palace et al. (2008).
h Clark et al. (2002).
i Delaney et al. (1998).
j Baker et al. (2007).
k Estimated.
l Selectively-logged forest.
m Mean of plot-based and transect-based methods.Table 5
Comparison of coarse woody debris in primary tropical forests in Asia and neotropics.
(see Table 2).
Site Fallen Standing
Necromass (Mg ha1)
ASIA
Bukit Timah 12.31 (8.40–19.37) 18.87 (5.84–23.49)
Pasoh, Malaysiaa – –
West Sumatrab 39.0 16k
Malua, Malaysiac,l 9.0 17.4
Belalong, Bruneid
Andalau, Bruneid
Danum, Malaysiad
NEOTROPICS
Jenaro Herrera, Perue 14.4 5.9
Porce, Colombiaf – –
Tapajos, Brazilg 40.8 8.1
K.M. Ngo et al. / Forest Ecology aThe increase in the soil carbon stock under secondary forest at
BTNR appears to be primarily due to an increase in soil carbon con-
centrations throughout the upper meter of soil associated with an
increase in fine root biomass. This suggests that fine root turnover
might contribute to the increase in soil carbon stocks. The soil car-
bon to nitrogen ratios were also higher in the secondary forest
compared to the primary forest, indicating less decomposed organ-
ic matter. In assessing the difference in soil carbon between the
primary and secondary forest plots it is important to consider land-
scape position – the primary forest plot is on top of a hill and in-
cludes a ridge with steeply sloping soils. A greater rate of erosion
might account for the lower carbon concentrations in the topsoil,
compared to more enriched sites lower down the slope where
the secondary plot is located.
5. Conclusion
This first quantification of carbon stocks in a Singapore forest
indicates a marked difference between primary and 60-year-old
secondary forests. Total carbon stocks were greater in primary for-
est than secondary forest, with the majority of carbon in primary
forest stored in aboveground biomass, while secondary forest soils
held the majority of the carbon. In general, carbon stocks in BTNR
forests are lower than other sites in Southeast Asia, but are compa-
rable to many neotropical forests. The importance of accounting for
carbon in deep subsoil (>1 m) is emphasized by the approximate
40% increase in soil carbon stocks when including soils to 3 m
depth.
Carbon stocks in the 60–70 year old secondary forests in BTNR
still lag well behind the adjacent primary forest. In secondary for-
ests, carbon stocks typically increase rapidly during the initial
phase of regeneration, and then decelerate over subsequent dec-
ades and even centuries as primary forest species graduallyes in parentheses indicate 95% confidence intervals based on 1000 bootstrap samples
Total Fallen Standing Total
anagement 296 (2013) 81–89 87colonize the area and grow to maturity. Given that primary forest
is in such close proximity to secondary forest in BTNR, the slow
dipterocarp recolonization at this site is surprising. This has impli-
cations for secondary forest management in Singapore and South-
east Asian forests. Active management, like enrichment planting,
might accelerate regeneration and carbon accumulation of second-
ary forests in BTNR.
Fig. 4. Comparison of soil carbon for the upper 1 m of soil in a range of tropical
forests in Asia, the neotropics, and the Hawaiian Islands. Locations are as follows:
1 = this study, 2 = Yonekura et al. (2010), 3 = de Camargo et al. (1999), 4 = Sommer
et al. (2000), 5 = Trumbore et al. (1995), 6 = Marin-Spiotta et al. (2009), 7–
8 = Veldkamp et al. (2003), 9 = this study, 10 = de Camargo et al. (1999), 11–
14 = Sommer et al. (2000), 15–16 = Osher et al. (2003).
30, 1489–1493.
nd MGibbon, A., Silman, M.R., Malhi, Y., Fisher, J.B., Meir, P., Zimmermann, M., Dargie,
G.C., Farfan, W.R., Garcia, K.C., 2010. Ecosystem carbon storage across the
grassland–forest transition in the high Andes of Manu National Park, Peru.
Ecosystems 13, 1097–1111.
Grace, J., 2004. Understanding and managing the global carbon cycle. Journal of
Ecology 92, 189–202.
Grubb, P.J., Turner, I.M., Burslem, D.F.R.P., 1994. Mineral nutrient status of coastal
hill dipterocarp forest and adinandra belukar in Singapore: analysis of soil,
leaves and litter. Journal of Tropical Ecology 10, 559–577.Acknowledgements
We thank Mohamad Fairoz bin Mohamed and other assistants
for help in the field, Ryan Chisholm for help with data analysis,
and Dayana Agudo for laboratory support. The research was
funded by the HSBC Carbon Initiative and a CTFS grant to K.M.N.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.foreco.2013.02.
004.
References
Alberton, O., Kuyper, T.W., Gorissen, A., 2005. Taking mycocentrism seriously:
mycorrhizal fungal and plant responses to elevated CO2. The New Phytologist
167, 859–868.
Baker, T.R., Honorio Coronado, E.N., Phillips, O.L., Martin, J., van der Heijden, G.M.F.,
Garcia, M., Silva Espejo, J., 2007. Low stocks of coarse woody debris in a
southwest Amazonian forest. Oecologia 152, 495–504.
Beer, C., Reichstein, M., Tomelleri, E., Ciais, P., Jung, M., Carvalhais, N., Rodenbeck, C.,
Altaf Arain, M., Baldocchi, D., Bonan, G.B., Bondeau, A., Cescatti, A., Lasslop, G.,
Lindroth, A., Lomas, M., Luyssaert, S., Margolis, H., Oleson, K.W., Roupsard, O.,
Veenendaal, E., Viovy, N., Williams, C., Woodward, F.I., Papale, D., 2010.
Terrestrial gross carbon dioxide uptake: global distribution and covariation
with climate. Science 329, 834–838.
Brown, S., Lugo, A.E., 1990. Tropical secondary forests. Journal of Tropical Ecology 6,
1–32.
Burslem, D.F.R.P., Turner, I.M., Grubb, P.J., 1994. Mineral nutrient status of coastal
hill dipterocarp forest and Adinandra belukar in Singapore: bioassays of
nutrient limitation. Journal of Tropical Ecology 10, 579–599.
Chao, K.-J., Phillips, O.L., Baker, T.R., 2008. Wood density and stocks of coarse woody
debris in a northwestern Amazonian landscape. Canadian Journal of Forest
Research 38, 795–805.
Chave, J., Cairns, M.A., Andalo, C., Brown, S., Chambers, J.Q., Eamus, D., Fölster, H.,
Fromard, F., Higuchi, N., Kira, T., Lescure, J.-P., Nelson, B.W., Ogawa, H., Puig, H.,
Riéra, B., Yamakura, T., 2005. Tree allometry and improved estimation of carbon
stocks and balance in tropical forests. Oecologia 145, 87–99.
Chave, J., Condit, R., Muller-Landau, H.C., Thomas, S.C., Ashton, P.S., Bunyavejchewin,
S., Co, L.L., Dattaraja, H.S., Davies, S.J., Esufali, S., Ewango, C.E.N., Feeley, K.J.,
Foster, R.B., Gunatilleke, N., Gunatilleke, S., Hall, P., Hart, T.B., Hernández, C.,
Hubbell, S.P., Itoh, A., Kiratiprayoon, S., Lafrankie, J.V., Loo de Lao, S., Makana, J.-
R., Noor, M.N.S., Kassim, A.R., Samper, C., Sukumar, R., Suresh, H.S., Tan, S.,
Thompson, J., Tongco, M.D.C., Valencia, R., Vallejo, M., Villa, G., Yamakura, T.,
Zimmerman, J.K., Losos, E.C., 2008. Assessing evidence for a pervasive alteration
in tropical tree communities. PLoS Biology 6, e45.
Clark, D.B., Clark, D.A., Brown, S., Oberbauer, S.F., Veldkamp, E., 2002. Stocks and
flows of coarse woody debris across a tropical rain forest nutrient and
topography gradient. Forest Ecology and Management 164, 237–248.
Corlett, R.T., 1992. The ecological transformation of Singapore, 1819–1990. Journal
of Biogeography 19, 411–420.
de Camargo, P.B., Trumbore, S.E., Martinelli, L.A., Davidson, E.A., Nepstad, D.C.,
Reynaldo, V.L., 1999. Soil carbon dynamics in regrowing forest of eastern
Amazonia. Global Change Biology 5, 693–702.
Delaney, M., Brown, S., Lugo, A.E., Torres-Lezama, A., Quintero, B.N., 1998. The
quantity and turnover of dead wood in permanent forest plots in six life zones
of Venezuela. Biotropica 30, 2–11.
Dixon, R.K., Solomon, A.M., Brown, S., Houghton, R.A., Trexler, M.C., Wisniewski, J.,
1994. Carbon pools and flux of global forest ecosystems. Science 263, 185–190.
Djomo, A.N., Knohl, A., Gravenhorst, G., 2011. Estimations of total ecosystem carbon
pools distribution and carbon biomass current annual increment of a moist
tropical forest. Forest Ecology and Management 261, 1448–1459.
Fontaine, S., Barot, S., Barré, P., Bdioui, N., Mary, B., Rumpel, C., 2007. Stability of
organic carbon in deep soil layers controlled by fresh carbon supply. Nature
450, 277–280.
Gale, N., 2000. The aftermath of tree death: coarse woody debris and the
topography in four tropical rain forests. Canadian Journal of Forest Research
88 K.M. Ngo et al. / Forest Ecology aIPCC, 2006. IPCC guidelines for national greenhouse gas inventories. In: Eggleston,
S., Buendia, L., Miwa, K., Ngara, T., Tanabe, K. (Eds.), vol. 4: Agriculture, Forestry
and Other Land Use. IGES, Japan.Ives, D.W., 1977. Soils of the Republic of Singapore. Lower Hutt, New Zealand.
Kenzo, T., Ichie, T., Hattori, D., Itioka, T., Handa, C., Ohkubo, T., Kendawang, J.J.,
Nakamura, M., Sakaguchi, M., Takahashi, N., Okamoto, M., Tanaka-Oda, A.,
Sakurai, K., Ninomiya, I., 2009. Development of allometric relationships for
accurate estimation of above- and below-ground biomass in tropical secondary
forests in Sarawak, Malaysia. Journal of Tropical Ecology 25, 371–386.
Kenzo, T., Ichie, T., Hattori, D., Kendawang, J.J., Sakurai, K., Ninomiya, I., 2010.
Changes in above- and belowground biomass in early successional tropical
secondary forests after shifting cultivation in Sarawak, Malaysia. Forest Ecology
and Management 260, 875–882.
Lafrankie, J.V., Davies, S.J., Wang, L.K., Lee, S.K., Lum, S.K.Y., 2005. Forest Trees of
Bukit Timah: Population Ecology in a Tropical Forest Fragment. Simply Green,
Singapore.
Larjavaara, M., Muller-Landau, H.C., 2009a. Woody Debris Research Protocol: CWD
Dynamics. Version January 2009.
Larjavaara, M., Muller-Landau, H.C., 2009b. Woody Debris Research Protocol: Long
Transects. Version November 2009.
Larjavaara, M., Muller-Landau, H.C., 2010. Comparison of decay classification, knife
test, and two penetrometers for estimating wood density of coarse woody
debris. Canadian Journal of Forest Research 40, 2313–2321.
Larjavaara, M., Muller-Landau, H.C., 2011. Cross-section mass: an improved basis
for woody debris necromass inventory. Silva Fennica 45, 291–298.
Lasco, R.D., Guillermo, I.Q., Cruz, R.V.O., Bantayan, N.C., Pulhin, F.B., 2004. Carbon
stocks assessment of a secondary forest in Mount Makiling Forest Reserve,
Philippines. Journal of Tropical Forest Science 16, 35–45.
Lewis, S.L., Lopez-Gonzalez, G., Sonké, B., Affum-Baffoe, K., Baker, T.R., Ojo, L.O.,
Phillips, O.L., Reitsma, J.M., White, L., Comiskey, J.A., Djuikouo, M.-N.K., Ewango,
C.E.N., Feldpausch, T.R., Hamilton, A.C., Gloor, M., Hart, T., Hladik, A., Lloyd, J.,
Lovett, J.C., Makana, J.-R., Malhi, Y., Mbago, F.M., Ndangalasi, H.J., Peacock, J.,
Peh, K.S.-H., Sheil, D., Sunderland, T., Swaine, M.D., Taplin, J., Taylor, D., Thomas,
S.C., Votere, R., Wöll, H., 2009. Increasing carbon storage in intact African
tropical forests. Nature 457, 1003–1006.
Lü, X.-T., Yin, J.-X., Jepsen, M.R., Tang, J.-W., 2010. Ecosystem carbon storage and
partitioning in a tropical seasonal forest in Southwestern China. Forest Ecology
and Management 260, 1798–1803.
Malhi, Y., Aragão, L.E.O.C., Metcalfe, D.B., Paiva, R., Quesada, C.A., Almeida, S.,
Anderson, L., Brando, P., Chambers, J.Q., Da Costa, A.C.L., Hutyra, L.R., Oliveira, P.,
Patiño, S., Pyle, E.H., Robertson, A.L., Teixeira, L.M., 2009. Comprehensive
assessment of carbon productivity, allocation and storage in three Amazonian
forests. Global Change Biology 15, 1255–1274.
Malhi, Y., Wood, D., Baker, T.R., Wright, J., Phillips, O.L., Cochrane, T., Meir, P., Chave,
J., Almeida, S., Arroyo, L., Higuchi, N., Killeen, T.J., Laurance, S.G., Laurance, W.F.,
Lewis, S.L., Monteagudo, A., Neill, D.A., Vargas, P.N., Pitman, N.C.A., Quesada,
C.A., Salomão, R., Silva, J.N.M., Lezama, A.T., Terborgh, J., Martínez, R.V., Vinceti,
B., 2006. The regional variation of aboveground live biomass in old-growth
Amazonian forests. Global Change Biology 12, 1107–1138.
Marin-Spiotta, E., Silver, W.L., Swanston, C.W., Ostertag, R., 2009. Soil organic matter
dynamics during 80 years of reforestation of tropical pastures. Global Change
Biology 15, 1584–1597.
Mascaro, J., Asner, G., Dent, D., DeWalt, S.J., Denslow, J.S., 2012. Scale-dependence of
aboveground carbon accumulation in secondary forests of Panama: a test of the
intermediate peak hypothesis. Forest Ecology and Management 276, 62–70.
NEA, n.d. Weather Statistics. <http://app2.nea.gov.sg/weather_statistics.aspx>.
Ng, F.S.P., Whitmore, T.C., 1989. Tree Flora of Malaya. Longman, Malaysia.
Niiyama, K., Kajimoto, T., Matsuura, Y., Yamashita, T., Matsuo, N., Yashiro, Y., Ripin,
A., Kassim, A.R., Noor, N.S., 2010. Estimation of root biomass based on
excavation of individual root systems in a primary dipterocarp forest in Pasoh
Forest Reserve, Peninsular Malaysia. Journal of Tropical Ecology 26, 271.
Osher, L.J., Matson, P.A., Amundson, R., 2003. Effect of land use change on soil
carbon in Hawaii. Biogeochemistry 65, 213–232.
Palace, M., Keller, M., Silva, H., 2008. Necromass production: studies in undisturbed
and logged Amazon forests. Ecological Applications 18, 873–884.
Pan, Y., Birdsey, R.A., Fang, J., Houghton, R., Kauppi, P.E., Kurz, W.A., Phillips, O.L.,
Shvidenko, A., Lewis, S.L., Canadell, J.G., Ciais, P., Jackson, R.B., Pacala, S.W.,
McGuire, A.D., Piao, S., Rautiainen, A., Sitch, S., Hayes, D., 2011. A large and
persistent carbon sink in the world’s forests. Science 333, 988–993.
Powers, J.S., Corre, M.D., Twine, T.E., Veldkamp, E., 2011. Geographic bias of field
observations of soil carbon stocks with tropical land-use changes precludes
spatial extrapolation. Proceedings of the National Academy of Sciences of the
United States of America 108, 10–14.
Saner, P., Loh, Y.Y., Ong, R.C., Hector, A., 2012. Carbon stocks and fluxes in tropical
lowland dipterocarp rainforests in Sabah, Malaysian Borneo. PloS One 7,
e29642.
Sierra, C.A., Del Valle, I.J., Orrego, S.A., Moreno, F.H., Harmon, M.A., Zapata, M.,
Colorado, G.J., Herrera, M.A., Lara, W., Restrepo, D.E., Berrouet, L.M., Loaiza,
L.M., Benjumea, J.F., 2007. Total carbon stocks in a tropical forest landscape
of the Porce region, Columbia. Forest Ecology and Management 243, 299–
309.
Slik, J.W.F., Aiba, S.-I., Brearley, F.Q., Cannon, C.H., Forshed, O., Kitayama, K.,
Nagamasu, H., Nilus, R., Payne, J., Paoli, G., Poulsen, A.D., Raes, N., Sheil, D.,
Sidiyasa, K., Suzuki, E., Van Valkenburg, J.L.C.H., 2010. Environmental correlates
of tree biomass, basal area, wood specific gravity and stem density gradients in
Borneo’s tropical forests. Global Ecology and Biogeography 19, 50–60.
anagement 296 (2013) 81–89Soil Survey Staff, 1999. Soil Taxonomy: A Basic System of Soil Classification for
Making and Interpreting Soil Surveys United States Department of Agriculture–
Natural Resources Conservation Service. Lincoln, NE.
Sommer, R., Denich, M., Vlek, P.L.G., 2000. Carbon storage and root penetration in
deep soils under small-farmer land-use systems in the Eastern Amazon region,
Brazil. Plant and Soil, 231–241.
Symington, C.F., Ashton, P.S., Appanah, S., 2004. Forester’s Manual of Dipterocarps.
Malaysian Nature Society.
Thomlinson, J.R., Serrano, M.I., del M. Lopez, T., Aide, T.M., Zimmerman, J.K., 1996.
Land-use dynamics in a post-agricultural Puerto Rican landscape (1936–1988).
Biotropica 28, 525.
Trumbore, S., Davidson, E., de Camargo, P.B., Nepstad, D.C., Martinelli, L.A., 1995.
Belowground cycling of carbon in forests and pastures of Eastern Amazonia.
Global Biogeochemical Cycles 9, 515–528.
Veldkamp, E., Becker, A., Schwendenmann, L., Clark, D.A., Schulte-Bisping, H., 2003.
Substantial labile carbon stocks and microbial activity in deeply weathered soils
below a tropical wet forest. Global Change Biology 9, 1171–1184.
Warren, W.G., Olsen, P.F., 1964. A line transect technique for assuming logging
waste. Forest Science 10, 267–276.
Wright, S.J., 2005. Tropical forests in a changing environment. Trends in Ecology &
Evolution 20, 553–560.
Yoneda, T., Yoda, K., Kira, T., 1977. Accumulation and decomposition of big
wood litter in Pasoh Forest, West Malaysia. Japanese Journal of Ecology 27,
53–60.
Yoneda, T., Tamin, R., Ogino, K., 1990. Dynamics of aboveground big woody organs
in a foothill dipterocarp forest, West Sumatra, Indonesia. Ecological Research 5,
111–130.
Yonekura, Y., Ohta, S., Kiyono, Y., Aksa, D., Morisada, K., Tanaka, N., Kanzaki, M.,
2010. Changes in soil carbon stock after deforestation and subsequent
establishment of ‘‘Imperata’’ grassland in the Asian humid tropics. Plant and
Soil 329, 495–507.
K.M. Ngo et al. / Forest Ecology and Management 296 (2013) 81–89 89