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Contents lists available at ScienceDirect

Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Below- and above-ground biomass and net primary production in a paleotropical

natural forest (Sulawesi, Indonesia) as compared to neotropical forests
D. Hertel a,*, G. Moser a, H. Culmsee b, S. Erasmi c, V. Horna a, B. Schuldt a, Ch. Leuschner a
a

Plant Ecology, Albrecht-von-Haller Institute for Plant Sciences, University of Gottingen, Untere Karspule 2, 37073 Gottingen, Germany
Vegetation and Phytodiversity Analysis, Albrecht-von-Haller Institute for Plant Sciences, University of Gottingen, Untere Karspule 2, 37073 Gottingen, Germany
c
Cartography, GIS and Remote Sensing, Institute of Geography, University of Gottingen, Goldschmidtstr. 5, 37077 Gottingen, Germany
b

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 10 February 2009
Received in revised form 1 July 2009
Accepted 8 July 2009

Data on the biomass and productivity of southeast Asian tropical forests are rare, making it difcult to
evaluate the role of these forest ecosystems in the global carbon cycle and the effects of increasing
deforestation rates in this region. In particular, more precise information on size and dynamics of the
root system is needed. In six natural forest stands at pre-montane elevation (c. 1000 m a.s.l.) on Sulawesi
(Indonesia), we determined above-ground biomass and the distribution of ne (d < 2 mm) and coarse
roots (d > 2 mm), estimated above- and below-ground net production, and compared the results to
literature data from other pre-montane paleo- and neotropical forests. The mean total biomass of the
stands was 303 Mg ha1 (or 128 Mg C ha1), with the largest biomass fraction being recorded for the
above-ground components (286 Mg ha1) and 11.2 and 5.6 Mg ha1 of coarse and ne root biomass
(down to 300 cm in the soil prole), resulting in a remarkably high shoot:root ratio of c. 17. Fine root
density in the soil prole showed an exponential decrease with soil depth that was closely related to the
concentrations of base cations, soil pH and in particular of total P and N. The above-ground biomass of
these stands was found to be much higher than that of pre-montane forests in the Neotropics, on
average, but lower compared to other pre-montane forests in the Paleotropics, in particular when
compared with dipterocarp forests in Malesia. The total above- and below-ground net primary
production was estimated at 15.2 Mg ha1 yr1 (or 6.7 Mg C ha1 yr1) with 14% of this stand total being
invested below-ground and 86% representing above-ground net primary production. Leaf production
was found to exceed net primary production of stem wood. The estimated above-ground production was
high in relation to the mean calculated for pre-montane forests on a global scale, but it was markedly
lower compared to data on dipterocarp forests in South-east Asia. We conclude that the studied forest
plots on Sulawesi follow the general trend of higher biomasses and productivity found for paleotropical
pre-montane forest compared to neotropical ones. However, biomass stocks and productivity appear to
be lower in these Fagaceae-rich forests on Sulawesi than in dipterocarp forests of Malesia.
2009 Elsevier B.V. All rights reserved.

Keywords:
Carbon partitioning
Coarse roots
Fine root system
Litter fall
Pre-montane rain forest
Shoot:root ratio
Stem increment

1. Introduction
Tropical forests are being destroyed at rapid rates (Nepstad
et al., 1999; Achard et al., 2002) with highest conversion rates in
South-east Asia (FAO, 2003). The importance of tropical rain forests
for the global atmospheric carbon cycle is well recognized and the
marked consequences of forest conversion for the carbon budget
have been frequently discussed (e.g. Raich, 1983; Smith et al.,
2002; Lal, 2005; Jandl et al., 2007). However, our knowledge on
biomass carbon pools and carbon xation with net primary
production of tropical forests is based on a relatively small number

* Corresponding author. Tel.: +49 551 395708; fax: +49 551 3922029.
E-mail address: dhertel@gwdg.de (D. Hertel).

of studies mostly from South and Central America, while precise

data from South-east Asia and Africa are rare. Moreover, most
reports focus on the carbon pools of the above-ground components
of rain forests alone, and studies that consider also the structure
and dynamics of the root system are scarce. This is all the more
problematic since particularly the ne roots (roots smaller than
2 mm in diameter) are known to play an important role in the
carbon budget of forests. Although tree ne roots account only for a
few percent of total tree biomass, they represent a signicant sink
for assimilates consuming up to an estimated 3050% of annual net
primary production (Keyes and Grier, 1981; Ruess et al., 1996; Vogt
et al., 1996; Xiao et al., 2003). Fine roots of tropical trees are
assumed to show particularly rapid growth rates and turnover, and
therefore to have a large inuence on ecosystem carbon uxes (e.g.
Silver et al., 2005).

0378-1127/$ see front matter 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2009.07.019

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

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Our study was conducted in six forest plots of a natural premontane tropical moist forest in Central Sulawesi (Indonesia),
which is characterized by tree species of tropical Fagaceae, a
widespread family in southeast Asian mountain forests that is also
abundant in extra-tropical regions. Our objective was to investigate the carbon pools and the carbon sequestration with primary
production in these forests stands. A main goal of the study is to
elucidate the contribution of the root system to the carbon budget
of the studied forest ecosystem. This was done not only for the
upper soil horizons but also for deeper layers (down to 300 cm)
close to the bedrock. The aims of the study were (i) to analyse the
vertical structure of the ne and coarse root system in their
relation to soil chemical properties, (ii) to inventory the aboveground biomass and related carbon pools by tree families, (iii) to
estimate the above- and below-ground net primary production,
and (iv) to compare the biomass and productivity of these forest
stands with data from other southeast Asian and also neo-tropical
pre-montane forests. To cope with the apparent differences of
these parameters among stands of markedly different climate
conditions, our study focuses on forests of the pre-montane zone
(4001200 m a.s.l., following the denitions given by Grubb
(1977), Whitmore (1984) and Richards (1996)), and only stands
from the tropical moist region (>1700 mm rainfall yr1 as dened
by Richards (1996)) were included in the comparison.
2. Materials and methods
2.1. Study site description
The study was conducted in a pre-montane rain forest in the
Lore Lindu National Park in Central Sulawesi, Indonesia (01829.60 S,
120803.40 E). This national park contains one of the largest
remaining areas of evergreen rain forest in the region. While
various land use practices with different degrees of forest
disturbance intensity are common in the margin zone, there are
still large areas of undisturbed natural forest left in the central
parts of the national park. In Pono Valley about 4 km NE of the
village of Toro, six study plots of 40 m  40 m each were selected in
the natural forest on the same hillside with low inclination located
at 1050 m elevation in an area of ca. 5 ha in close vicinity to each
other (maximum distance ca. 250 m) to guarantee comparable site
conditions. All stands were on Ferralsol soils (FAO-classication,
Leitner and Michalzik, unpubl.) derived from metamorphic bedrock on gentle slopes (inclination 0208). The soils were
moderately nutrient-rich with pH(H2O) values of 4.4, a cation
exchange capacity of c. 600 mmolc g1, base saturation of c. 22%, a
nitrogen concentration of 2 mg g1 and a C:N ratio of 13 in the
upper 20 cm of the mineral soil (Leitner and Michalzik, unpublished). Mean annual temperature during the study period (March
2007 to February 2008) measured on a 14 m high tower within a
gap close to the sites was 20.8 8C, and annual rainfall during this
period was 3534 mm.

revealed that the vast majority of the roots were alive at the time of
extraction from the soil, thus represented root biomass. However, a
small fraction (a few percent) of the ne and coarse root mass
extracted in this way may be attributed to the dead root fraction
(indicated by signs of death roots, e.g. non-turgescence, disintegration of stele and cortex, etc., see for Leuschner et al., 2001).
After drying at 70 8C to constant mass, all samples were weighed
and the data were expressed as ne and coarse root density (g L1)
per soil depth and as root biomass total (g m2) of the soil prole
(to 300 cm). We have to state here that below-ground stumps of
the trees were not covered with this method, hence leading to an
underestimation of the total below-ground biomass. The carbon
concentration of the ne and coarse root samples was measured
with a CN auto-analyzer (Vario EL III, Hanau, Germany) at the
University of Gottingen in order to estimate the carbon pools in the
ne and coarse root system.
2.3. Estimation of ne root production
An ingrowth core experiment was established in three of the six
study plots to estimate annual ne root production (Powel and
Day, 1991; Godbold et al., 2006). Six soil cores (67 mm in diameter
and 20 cm in depth) were taken in February 2007 from randomly
distributed locations within each study plot. All visible ne roots
(>10 mm length) were carefully removed from the soil material
and the root-free material was replaced into the hole. Care was
taken that as much as possible of structure and density of the soil
samples was conserved. The ingrowth cores were marked at the
soil surface with PVC tubes. The cores were recollected after 16
months in order to measure the regrowth of roots into the soil. In
the laboratory, the samples were washed and all ne roots
(>10 mm length) were extracted by hand, washed and dried
(70 8C, 48 h). Following Vogt et al. (1998), we equalled annual ne
root production with the ne root mass (living and dead) at harvest
in the cores related to the time span between the start of
recolonization and harvest. Earlier studies in nearby forest plots
had shown that ne root recolonization of the cores started about 2
months after the installation of the ingrowth cores (due to the
initial soil disturbance) and that root mortality and hence mass and
decomposition of dead root was low in these cores (Leuschner
et al., 2009). Thus, we assumed that the ne root biomass recorded
in the cores 16 months after the installation of the cores reected a
ne root growth period of 14 months. Fine root growth in the cores
was extrapolated to 1 year and expressed in g m2 yr1. By relating
the ne root growth in the ingrowth cores to the existing ne root
biomass in the upper 20 cm of the soil as measured during root
inventory, we obtained the ne root growth rate. For estimating
the annual ne root production in the soil prole to 300 cm depth,
we extrapolated the growth rates of 020 cm horizon to the root
mass to lower horizons.
2.4. Above-ground stand structure, biomass, and annual primary
production

2.2. Analysis of vertical ne and coarse root biomass distribution

At a minimum distance of 1 m to the next tree (dbh > 10 cm),
two soil pits per plot were dug down to 300 cm depth in January
and February 2007. Soil monoliths of a volume of 40 cm  40 cm
and 20 cm depth were extracted subsequently at 20 cm depth
intervals from one of the prole walls to record the vertical
distribution of ne roots (diameter < 2 mm) and large and coarse
roots (d > 2 mm) in the soil. The soil of the monoliths was sieved
(mesh size: 3 mm) and all visible root branches were transferred
into plastic bags and were taken to the laboratory of the University
Tadulako in Palu, were they were washed and sorted into ne and
coarse roots. Microscopic inspection of selected ne root samples

In August and September 2006, a stand inventory was carried

out in the six study plots of 0.16 ha each. A 10 m  10 m grid was
laid on the 40 m  40 m plots and all trees with diameter at breast
height (dbh at 1.3 m)  10 cm were tagged within each of the
10 m  10 m subplots, their plot coordinates determined, the dbh
measured with a measuring tape (Richter Measuring Tools,
Speichersdorf, Germany) and tree height recorded using a Vertex
III height meter (Haglof, Langsels, Sweden). If buttresses or stilt
roots were present, dbh was measured above them according to
the recommendations for tree diameter measurement given by
Clark et al. (2001b). To survey understorey trees of 29.9 cm in
dbh, an area of 5 m  5 m was demarcated in each of the

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

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10 m  10 m subplots and surveyed as described for the large

trees.
Tree species identication was based on voucher specimens
collected from tagged trees and supplementary trees inspected
in ower or fruit. Less than 1% of the individuals remained
unidentied. Species were assigned to families according to The
International Plant Names Index (IPNI, 2008). Details on species
identication and description, deposition of vouchers at herbaria
and the complete species list of the study site are given in
Culmsee and Pitopang (2009) and Culmsee (2008). A samplebased rarefaction analysis (Gotelli and Colwell, 2001) revealed
that the sampled area was sufcient to reach the plateau
segments of the respective speciesarea curves (Culmsee and
Pitopang, 2009).
For the conversion of the recorded tree structural data into
above-ground biomass, we obtained the wood-specic gravity r
for the observed species/genera from various sources (Soerianegara and Lemmens, 1993; Lemmens et al., 1995; Sosef et al., 1998;
Oey, 1990) and applied the allometric equation of Chave et al.
(2005) for tropical wet stands:
AGB exp2:557 0:940 lnr D2 H

(1)

where AGB is the estimated above-ground biomass (in kg per tree,

including stem and branch wood and leaf biomass), D the trunk
diameter (dbh in cm), H total tree height (in m), and r woodspecic gravity (in g cm3). The literature data on wood density
used for our calculation often refer to wood samples measured
under fresh weight conditions (i.e. at 12 or 15% moisture). To
transform these data to wood-specic gravity on a dry weight
basis, we transformed the literature data following Chave et al.
(2006). In cases, where ranges of wood density values were
reported, we used median values. Where wood density data were
unavailable for a species, the average across all species in that
genus growing in the corresponding habitat was applied (see Baker
et al., 2004; Slik, 2006). In the few cases, where a tree individual
could not be identied at least to the genus level or where not
literature record was available, we used the plot average.
Due to their specic growth forms, two taxa required a specic
calculation procedure for estimating AGB. (1) Castanopsis acuminatissima Blume (Fagaceae) is a frequent tree species that builds
clusters of root suckers sprouting from a common compact basis of
up to 2 m height (Soepadmo, 1972). Each stem of 2 cm dbh was
measured above this common basis of 2 m height and AGB was
calculated separately for each stem. (2) Stranglers of the genus
Ficus L. (Moraceae, n = 3) that have developed to a free-standing
tree-like structure are characterised by a large hole amidst of the
vertical axis that was originally lled by the trunk of the host tree.
The above-ground biomass of these stranglers was estimated by
calculating the AGB for both the strangler and the original host tree
and subsequently subtracting the latter from the former. The
specic calculation of stranglers AGB was documented by Culmsee
et al. (submitted).
In order to estimate leaf biomass, we used LAI data together
with data on specic leaf area SLA obtained from litter traps
installed in every plot (see below). LAI values were derived from
hemispherical photographs taken at 1 m height at 12 points per
plot at regular grid positions. The program CanEye was used for
image analyses and the effective LAI (LAIeff) for a zenith angle of
57.58 was calculated after Bonhomme and Chartier (1972); LAI true
(LAItrue) was derived from the expression LAItrue = LAIeff/CI with the
clumping index (CI) being calculated for each image after Lang and
Xiang (1986). With the LAI and SLA data, we obtained the standing
leaf biomass BL (g m2) from
BL LAI  SLA1

(2)

Annual above-ground tree biomass production (Mg ha1 yr1) was

estimated from stem increment data based on dendrometer tapes
(UMS, Germany) that were installed in December 2006 on 20 tree
individuals per study plot varying in dbh from 10 to 150 cm.
Cumulative increment from March 2007 to February 2008 was
used to calculate mean annual wood production for the tree
individuals and for all trees of a family in the six plots based on the
allometric regressions used for biomass estimation as described
above. For the tree individuals of all families not included in the
dendrometer study we applied increment rates that were
proportional to their wood density. Tree death did not occur in
our study; hence, a loss of tree wood biomass due to tree mortality
possibly occurring over a longer investigation period is not
considered in our calculations.
In order to estimate annual leaf production, 12 litter traps
(75 cm  75 cm aperture) per plot were installed in March
2007. The litter was collected every 2 weeks and sorted into
leaves and other ne litter components (in particular owers,
fruits and small twigs). At every second sampling date, all leaves
were scanned with a at bed scanner to determine the leaf area
using the software WinFolia 2000a (Regent Instruments,
Quebec, Canada). Specic leaf area (SLA) was calculated by
relating measured leaf area to the corresponding dry weight
(48 h, 70 8C). We assumed for this aseasonal forest that LAI
remained constant throughout the year and that all shed
leaves are immediately replaced by new ones. Thus, annual
leaf production should equal measured annual leaf litter
production.
For calculating the carbon stored in plant biomass and for
expressing net primary production into its components in terms of
C uxes, the C concentration of stem wood and litter was analyzed
with a CN auto-analyzer (Vario EL III, Hanau, Germany) at the
University of Gottingen.
2.5. Statistical analyses
Relationships between ne root density in the soil at different
depths and various chemical variables were analysed by simple
non-linear regression analysis using the software package Xact
(version 7.12, SciLab, Hamburg, Germany).
The non-parametric U-test after Mann and Whitney was used in
the literature meta-analysis to detect statistically signicant
differences between paleotropical and neotropical above- and
below-ground biomass or production. This test was carried out
with the software package SAS, version 8.2 (SAS Institute Inc., Cary,
NC, USA).
3. Results
3.1. Vertical structure of the ne and the coarse root system
The six forest plots showed a strong vertical decrease in ne
root biomass density with increasing soil depth (Fig. 1a). At 20
40 cm and 4060 cm depth, ne root density was reduced to only
16.5% and 6% of the density at 020 cm depth, respectively. Fine
root density decreased even further in the soil prole down to
300 cm. However, there was a small but notable amount of ne
root biomass found as deep as 300 cm in the soil reaching densities
< 0.01 g L1 (<10 g m3). Hence, c. 74% (i.e. 412 g m2) of the total
ne root biomass in the soil prole was found in the upper 20 cm of
the soil and >95% (representing 530 g m2) was present in the
upper 100 cm of the soil.
Coarse root biomass density (diameter > 2 mm) decreased
more rapidly with depth than that of ne root biomass (Fig. 1b).
Coarse root density declined to 8% and <2% at 2040 and
4060 cm, respectively, compared to the density in the topsoil

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

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Fig. 1. Vertical decrease in the density (biomass per soil volume) of ne (a, diameter < 2 mm) and coarse roots (b, diameter > 2 mm) in soil proles of the six forest plots at
Pono valley (Central Sulawesi) (means  SE of 20 cm  20 cm soil monolith data obtained from each two soil pits per plots; n = 12).

(020 cm). At 6080 cm depth, only 0.5% of the coarse root density
in the uppermost layer was present, and no coarse root biomass at
all was found at soil layers deeper than 80 cm. Accordingly, 91% of
the total coarse root biomass in the soil proles was located in the
upper 20 cm of the soil (i.e. 1060 g m2). Since all soil pits were
more than 1 m apart from the next large tree stem, large root
stocks are not covered by our analysis.
3.2. Interrelations between vertical ne root distribution and soil
properties along the prole
The strong exponential decrease in ne root biomass with
increasing soil depth was accompanied by marked changes in soil
chemical properties. Our analysis revealed a signicant positive
correlation between ne root biomass density and most of the
tested soil chemical variables except that of cation exchange
capacity (Table 1). While pH(H2O) was negatively correlated with
ne root biomass density in the soil, all other parameters were
positively correlated. However, since the absolute variation in
pH(H2O) values, cation exchange capacity, base saturation and
extractable Mg and Ca concentrations with increasing soil depth
were only small, the strongest relationship was found between ne
root biomass density and the carbon and nitrogen concentration
(and to a smaller degree the phosphorous and potassium
Table 1
Results from linear or simple non-linear regression analyses on the dependence of
ne root density at different soil depths on various soil parameters in the six natural
forest plots at Pono valley (Central Sulawesi). Given are r2adj. and P values and the
direction of the relationship. The analysis based on means (ne root biomass
density and soil parameters) over six forest plots, each with two soil pits.
Synchronous data on ne root biomass and soil chemistry were available from six
soil depths down to 260 cm. Soil chemical data were kindly provided by Leitner and
Michalzik (unpublished); C, N, and P data refer to total concentrations.
Source

Direction
of relationship

r2adj.

Soil depth
pH(H2O)
C (mg g1)
N (mg g1)
P (mg g1)
Cation exchange capacity (mmolc g1)
Base saturation (%)
Kextr (mmolc g1)
Mgextr (mmolc g1)
Caextr (mmolc g1)

+
+
+
+
+
+
+
+

0.99
0.86
0.99
0.99
0.99
0.46
0.99
0.99
0.44
0.99

<0.001
<0.001
<0.001
<0.001
<0.001
n.s.
<0.01
<0.001
<0.05
<0.001

concentration) in the soil. Almost the entire variability in the ne

root biomass density could be explained by the variation in the total
nitrogen concentration in the respective soil layers applying a nonlinear regression equation to the data (Fig. 2a). On the other hand,
the decrease in soil carbon content with increasing soil depth
appeared to be primarily a result of the decrease in ne root biomass
in the soil prole as it is suggested by the tight relationship of both
parameters found in the correlation analysis (Fig. 2b).
3.3. Above-ground forest structure
Mean tree height of all stems thicker than 2 cm in diameter was
c. 14 m in the six study plots and upper canopy height of the forest
plots was c. 29 m (Table 2). However, several very tall trees reached
more than 50 m in height, mostly individuals of C. acuminatissima.
Mean stem density was 870 trees per hectare (dbh > 10 cm) and
the mean basal area of the plots was 40 m2 ha1 (Table 2).
3.4. Above- and below-ground standing tree biomass and carbon
stocks
The ne and coarse root inventories and above-ground structural
investigations of the six forest plots together with biomass estimates
from above-ground allometric regression models allowed for a
comparison of above- and below-ground biomass fractions and
carbon pools. Accordingly, mean total phytomass (above- and
below-ground) of the stands was 302.7 Mg ha1, which is equivalent
to a carbon storage of 128 Mg ha1 (Table 3). The shoot:root ratio of
tree biomass was c. 17 with stem- and branch-wood representing
92% of the total phytomass (and 91% of the total tree carbon stock).
Coarse root biomass accounted for only 4% of the total phytomass.
The leaf biomass of the stands was somewhat larger than the ne
root biomass with the ratio of leaf to ne root biomass being 1.2. Fine
roots represented 1.8% of the stands biomass or tree carbon stock
totals.
Table 2
Above-ground stand structural attributes of the six natural forest
plots at Pono valley (Central Sulawesi). Given are means  SE;
only trees with dbh > 10 cm are considered.
Tree height (m)
Maximum tree height (m)
Stem density (trees ha1)
Basal area (m2 ha1)

13.9  10.3
38.8  1.5
869  50
40.3  1.6

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

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Fig. 2. Relationship between ne root density (biomass per soil volume) at different depths of the prole and soil N or C concentration at this depth of the six forest plots at
Pono valley (Central Sulawesi). In two soils proles analysed in each of the six natural forest plots (n = 12, 6 soil depths); (a) ne root density in relation to soil N concentration,
(b) soil C concentration (SOC) in relation to the ne root density. Soil C and N concentrations were measured from soil samples extracted in the same soil pits.

3.5. Above- and below-ground net primary production and carbon

partitioning to different organs
Tree species identication, as a basis for the estimation of the
above-ground net primary production, revealed that trees of 42
different families occurred in the six forest plots with a total area of
0.96 ha. Seventeen of these families were present with tree
individuals that accounted for more than 1% of the total stand basal
area (Table 4). Among them, trees from the Fagaceae showed the
highest portion of the standing basal area (>20%), followed by trees
from the Moraceae and the Sapotaceae (both representing more
than 10% of the basal area). Similarly, trees of the Fagaceae family
showed the highest annual increment of their basal area followed
by trees of the two other families. Annual wood biomass
production was also highest in trees of the Fagaceae followed
by the members of the Sapotaceae. In contrast, annual wood
biomass production of the tree-like structured individuals of the
genus Ficus (Moraceae) was very low due to the unusual shape of
Ficus sp. Moreover, trees from several other families that were less
abundant in terms of their contribution to the stand total basal
area (e.g. Lauraceae, Meliaceae, Euphorbiaceae) had relatively high
wood biomass production.
In order to estimate below-ground primary production, we
used an ingrowth core approach over a period of 16 months to
measure ne root growth in three of the six plots. The results of this
investigation may give a rough estimate of ne root growth. The
annual ne root production in the ingrowth cores amounted at
155 g m2 yr1 in the upper 20 cm of the soil. By applying the same
specic root growth rate found in this part of the prole to the ne
root density at deeper soil layers, we obtained an annual ne root
production of 209 g m2 yr1 for the entire soil prole (down to
300 cm soil depth).
Table 3
Above- and below-ground biomass and carbon pools by fraction in six natural forest
plots at Pono valley (Central Sulawesi) as estimated by above-ground structural
inventories in combination with allometric regression models, and coarse and ne
root biomass inventories (down to 300 cm soil depth). Given are means  SE. Please
note that below-ground stumps are not included in this data leading to an
underestimation of the total below-ground biomass.
Biomass fraction

Biomass (Mg ha1)

Carbon (Mg ha1)

Leaves
Stems and branches
Coarse roots
Fine roots
Total above-ground biomass
Total below-ground biomass
Total biomass
Leaf:ne root ratio
Shoot:root ratio

6.73  0.35
278.8  30.3
11.68  6.55
5.55  0.97
285.5  30.3
17.2  5.4
302.7
1.21
16.6

3.20  0.17
116.7  12.7
5.52  3.09
2.40  0.42
120.0  12.7
7.9  2.5
127.9
1.33
15.2

The total (above- and below-ground) primary production

of the trees was 15.2 Mg ha1 yr1, which is equivalent to an
annual carbon sequestration of 6.7 Mg ha1 yr1 (Table 5). The
most prominent carbon sink was found to be leaf growth that
accounted for 41.8% of the total net primary production (i.e.
2.6 Mg C ha1 yr1), followed by estimated stem (and branch)
increment (37%). Fine root production represented 13.8% of
annual net primary production representing a carbon allocation of
0.9 Mg C ha1 yr1 to root growth. While the shoot:root biomass
ratio was very high with about 17, about 6.2 times more carbon
was invested in the growth of above-ground organs than in roots
according to our calculations.
4. Discussion
4.1. Above- and below-ground biomass in tropical pre-montane moist
forests: a pan-tropical comparison
Due to their prominent role in the global carbon cycle, a more
accurate quantication of the biomass stocks and net primary
Table 4
Contribution of the most important families to the average stand totals of basal
area, basal area increment and estimated wood mass production in the six forest
plots at Pono valley (Central Sulawesi). Only families with more than 1%
contribution to the stand basal area are considereda.
Family

Relative
contribution
to stand basal
area (%)

Basal area
increment
(m2 ha1 yr1)

Wood mass
production
(Mg ha1 yr1)

Fagaceae
Moraceae
Sapotaceae
Lauraceae
Meliaceae
Burseraceae
Euphorbiaceae
Myrtaceae
Elaeocarpaceae
Icacinaceae
Myristicaceae
Clusiaceae
Compositae
Annonaceae
Rubiaceae
Rosaceae
Magnoliaceae

21.3
12.0
10.8
4.8
3.6
3.5
2.9
2.9
2.6
2.3
2.1
1.5
2.0
1.6
1.2
1.1
1.0

0.3440
0.1252
0.1195
0.0503
0.0407
0.0371
0.0329
0.0329
0.0291
0.0241
0.0239
0.0238
0.0214
0.0167
0.0125
0.0130
0.0104

1.7204
0.0025
0.9898
0.3647
0.3356
0.2443
0.3207
0.2310
0.2131
0.1144
0.1205
0.2379
0.1094
0.0831
0.0633
0.1199
0.0718

a
Families with less than 1% contribution to stand basal area were: Aceraceae,
Apocynaceae, Araliaceae, Arecaceae, Chrysobalanaceae, Cyatheaceae, Dracaenaceae, Escalloniaceae, Gesneriaceae, Himantadraceae, Juglandaceae, Lauraceae,
Leguminosae/Mimosoideae, Melastomataceae, Monimiaceae, Myrsinaceae, Oleaceae, Pandanaceae, Rhizophoraceae, Rutaceae, Sabiaceae, Sapindaceae, Staphyleaceae, Sterculiaceae, Theaceae, Verbenaceae.

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

G Model

FORECO-11765; No of Pages 9
D. Hertel et al. / Forest Ecology and Management xxx (2009) xxxxxx

Table 5
Net primary production (March 2007 to February 2008) in terms of dry mass or
carbon by biomass fraction in the six natural forest plots at Pono valley (Central
Sulawesi) (means  SE). No data are available for the large and coarse root production,
root exudation, transfer to mycorrhizal hyphae and consumption by herbivores. Leaf
production was thought to equal annual leaf litter fall (as long as no unusual dry spell
increases leaf fall). Fine root production was estimated from an ingrowth core
approach in three of the six plot scaled to the entire prole by vertical root biomass
distribution.
Biomass fraction

Biomass production
(Mg ha1 yr1)

Carbon production
(Mg ha1 yr1)

Leaves
Other ne litter fractions
Stems and branches
Fine roots
Total above-ground
Total below-ground
Stand total
Leaf:ne root ratio
Shoot:root ratio

6.35  0.90
1.17  0.27
5.62  0.27
2.09  0.21
13.1  0.6
2.1  0.2
15.2
3.04
6.2

2.60  0.43
0.51  0.12
2.65  0.13
0.90  0.09
5.8  0.3
0.9  0.1
6.7
2.89
6.4

production of tropical moist forests has attracted increasing

attention in the past decade (Lugo and Brown, 1992; Dixon et al.,
1994; Skole et al., 1998; Malhi and Grace, 2000; Clark, 2004). Large
effort has been done in the past years to identify and to minimize
possible errors in estimates of forest biomass and productivity
from eld measurements (e.g. Brown et al., 1995; Clark et al.,
2001b; Keller et al., 2001). Accordingly, our data set may be biased
by the lack of estimates of some components of the stand total
biomass (in particular that of below-ground stumps) or production
(e.g. leaf herbivory, rhizodeposition and C transfer to mycorrhizal
fungi). This clearly should have led to a certain underestimation of
the total tree biomass and productivity in our study. On the other
hand, large uncertainties that have been described to appear
frequently in applying allometric models for calculating aboveground biomass of tropical forests (e.g. Keller et al., 2001) should
have been mainly prevented in our study by including the woodspecic gravity for the present species/genera separately in the
allometric equation. Additionally, we included even small trees (up
to 2 cm dbh) in our allometric survey that also should have led to a
more accurate estimation of the above-ground biomass. Although
our single plot size was relatively small (c. 0.16 ha), the coefcient
of variance (CV) of the total above-ground biomass among the six
forest plots with a total area of ca. 1 ha was rather small (c. 25%)
and even lower than expected by the simulation model for the
dependence of the CV of tree biomass on the plot size in an
extensive methodological survey in a tropical rain forest in
Amazonia by Keller et al. (2001).
Studies on biomass stocks and productivity of natural forests
are very unevenly distributed throughout the tropical forest realm
with the majority of investigations being conducted in South and
Central America, while only few studies have been done in tropical
moist forests of South-east Asia (see the review by Clark et al.,
2001a). The southeast Asian rain forests are renowned for some
unique characteristics in their tree species composition, in
particular the abundance of Dipterocarpaceae in the lowland
forests of Malesia and of tropical Fagaceae in the mountain forests
(Whitmore, 1984; Ashton, 1988; Corlett, 2007). However, the
existing data have not been analysed satisfyingly to test the
hypothesis whether these oristic characteristics lead to deviating
biomass and productivity patterns in South-east Asia as comparing
to the Americas.
In their extended review of available literature data, Clark et al.
(2001a) give a broad range of 46694 Mg ha1 for the aboveground biomass of tropical forests globally. The mean value of this
data base (39 data sets) was 278 Mg ha1, which is surprisingly
similar to the value of 286 Mg ha1 recorded for our forest plots on
Sulawesi. However, for a more thorough comparison, the different

altitudinal position of the forest stands should be taken into

consideration since it has been shown that the above-ground
biomass declines with increasing elevation (Weaver and Murphy,
1990; Raich et al., 1997; Aiba and Kitayama, 1999; Kitayama and
Aiba, 2002; Moser et al., 2008). We used a large data set on tropical
moist forests reviewed by Hertel and Leuschner (in press) together
with some additional data to restrict the forest biomass data to the
pre-montane forest belt by using a conservative selection criterion
of 4001200 m a.s.l. (as a mean range from altitudinal zonation
models introduced by different authors for tropical moist forests
around the globe). For this more restricted data set, we found a
markedly lower mean above-ground biomass of 180 Mg ha1 for
neotropical moist pre-montane forests (n = 5) compared to
316 Mg ha1 for paleotropical forests (n = 8; Table 6). The two
forest stands from South-east Asia in the paleotropical data set (at
Mt Kinabalu, Sabah, Malaysia) showed particularly high aboveground biomass values: with an average of 496 Mg ha1, these premontane forests had a >80% higher above-ground biomass than
our forest plots on Sulawesi. This is an interesting nding since the
Sulawesi forest plots differ from those at Mt Kinabalu by the lack of
species from Dipterocarpaceae while the forests at both locations
contained several Fagaceae species, which are characteristic of
southeast Asian mountain forests. This oristic difference is due to
the historical biogeographical separation of the eastern Malesia
(including Sulawesi and New Guinea) from western Malesia by the
Wallaces line. While Borneo represents a hotspot of the diversity
of Dipterocarpaceae and Fagaceae species, only few species of
these families are abundant in Sulawesi and no dipterocarp species
reaches elevations above 500 m a.s.l. there (Ashton, 1982; Manos
and Stanford, 2001; Keler et al., 2002; Ashton, 2003). Hence, one
may speculate that the presence of the dipterocarp trees in the Mt
Kinabalu stands may have contributed to the marked difference in
above-ground biomass between both locations, e.g. by formation
of taller trees and/or by higher wood densities of the trees from the
Dipterocarpaceae. This is at least partly conrmed by a recent
study on allometric equation models for above-ground biomass
estimates of dipterocarp forest trees in Borneo that showed
particularly high wood densities (mean value 0.68 g cm3) for six
different Dipterocarpus species (Basuki et al., 2009).
The contribution of the root system to the stand total of biomass
is generally much smaller than that of the above-ground
components (Vogt et al., 1996). The 17 Mg ha1 of dry mass
recorded in our study on Sulawesi are relatively low compared to
the range of 1061 Mg ha1 and in relation to the mean value of
49 Mg ha1 given for tropical rain forests globally in the review of
literature data by Vogt et al. (1996) and Jackson et al. (1996),
respectively. One reason for this difference may be found in the fact
that no root stocks were excavated in our study. Thus, the recorded
root biomass values in the Sulawesi forest plots most likely
underestimate the actual total root biomass noticeably. On the
other hand, data from two other studies in southeast Asian rain
forests showed relatively low values of below-ground tree biomass
as well: Kira (1978) found 20 Mg ha1 in a Malaysian lowland rain
forest and Edwards and Grubb (1977) give a value of 28 Mg ha1
for a montane forest in New Guinea. Hence, these two studies
together with our results from the Sulawesi forest give some
evidence that the relatively low below-ground biomass in southeast Asian forests is in marked contrast to the high above-ground
tree biomass of these stands.
4.2. Above- and below-ground productivity and associated carbon
partitioning in the pre-montane rain forest on Sulawesi
Detailed investigations on the productivity of tropical moist
forests are still infrequent, particularly on the below-ground
component. Moreover, many of the existing studies missed to

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

G Model

FORECO-11765; No of Pages 9
D. Hertel et al. / Forest Ecology and Management xxx (2009) xxxxxx

Table 6
Above-ground biomass, above-ground production, and below-ground production of paleotropical (Paleo) and neotropical (Neo) mature natural rainforests of the premontane zone (4001200 m a.s.l.). The data were mainly extracted from the literature review by Hertel and Leuschner (in press), where further details on the location and the
site conditions of the stands are given.
Location

Biogeographical
afliation

Above-ground
biomass (Mg ha1)

Above-ground
production
(Mg ha1 yr1)

SW Cameroon
India (Kodayar)
India (Kodayar)
Malaysia (Mt Kinabalu)
Malaysia (Mt Kinabalu)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
USA (Hawaii)
Mexico (Los Tuxtlas)

Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Paleo
Neo

600

554
437

145
206
178
266
139

17.2
19.1
10.5
8.0
9.7
9.0
7.9
10.4
8.3
13.8
14.1

S Ecuador
Puerto Rico
Puerto Rico
Puerto Rico
Puerto Rico
Venezuela
means  SE of Paleotropical forests
means  SE of neotropical forests
This study (means  SE, n = 6)

Neo
Neo
Neo
Neo
Neo
Neo

190
197
148
172
194

316  66
180  9
286  30

9.4

11.4  1.3
11.7  2.3
13.1  0.6

Below-ground
production
(Mg ha1 yr1)

2.2
2.3

1.7
0.8
1.7
8.4
7.0
5.1
6.2
5.5
2.0
1.7

11.1
4.1  0.8
4.9  3.1
2.1  0.2

References

Ibrahim et al. (2002)

Sundarapandian and Swamy (1996)
Sundarapandian and Swamy (1996)
Kitayama and Aiba (2002)
Kitayama and Aiba (2002)
Ostertag (2001)
Ostertag (2001)
Ostertag (2001)
Herbert and Fownes (1999)
Herbert and Fownes (1999)
Herbert and Fownes (1999)
Herbert and Fownes (1999)
Herbert and Fownes (1999)
Sanchez-Gallen and
Alvarez-Sanchez (1996)
Moser et al. (unpublished)
Ovington and Olson (1970)
Edwards and Grubb (1977) a
Edwards and Grubb (1977) a
Edwards and Grubb (1977) a
Priess and Then Folster (1999)

Calculated based on data given by Briscoe and Wadsworth (1970).

investigate more than one or two prominent components of the

total net primary production in stands (see data reviewed by Clark
et al., 2001a).
For the above-ground biomass production of tropical forests, a
global mean of 8.8 Mg ha1 yr1 (equivalent to 4.4 Mg carbon
ha1 yr1) can be calculated from data sets of those studies
reviewed by Clark et al. (2001a) that directly measured aboveground biomass increment as well as ne litter fall (the two most
prominent components in estimates of above-ground net primary
production). This is signicantly lower than the above-ground
biomass production of 13.1 Mg ha1 yr1 (or 5.8 Mg C ha1 yr1)
recorded in our study plots on Sulawesi (P < 0.05). When conning
the comparison of the data sets to the pre-montane elevation zone
(as dened above), the mean value calculated from the modied
data base of Clark et al. (2001a) with 8.6 Mg ha1 yr1 did not differ
from the mean value for the whole altitudinal range. However, a
generalization from this nding is clearly hampered by the fact that
this conned data set exclusively comprised studies on the premontane zone of the Hawaiian islands. When using the data set on
tropical moist forests reviewed by Hertel and Leuschner (in press)
that contains a larger number of studies in pre-montane tropical
moist forests, we found a mean of 11.7 and 11.4 Mg ha1 yr1 for
above-ground biomass production of pre-montane neotropical and
paleotropical rain forests, respectively, which is more similar to the
value recorded in the Sulawesi plots (Table 6). Studies on the
productivity of southeast Asian moist forests are rare, but as for
above-ground biomass, it appears that pre-montane forests in
Malaysian (Mt Kinabalu) dipterocarp forests have an extraordinarily
high above-ground biomass production: with a mean of
18.1 Mg ha1 yr1, these stands showed markedly higher aboveground productivity than the Sulawesi forest. The particularly high
above-ground productivity of the pre-montane dipterocarp forests
on Mt Kinabalu is supported by the value of 16 Mg ha1 yr1
recorded in a Malaysian lowland dipterocarp forest (Kira, 1978). A
comparison of the most prominent components of above-ground
primary production wood increment and leaf litter production

suggests that dipterocarp forests are characterized by a relatively

high production of wood biomass compared to leaf biomass. The two
dipterocarp forests on Mt Kinabalu showed wood production of
7.0 Mg ha1 yr1 (Kitayama and Aiba, 2002) while the Sulawesi
forest plots, where dipterocarp species are absent but Fagaceae
species are dominant, showed a wood mass production of
5.6 Mg ha1 yr1. On the other hand, wood biomass production in
a neotropical pre-montane forest in Ecuador (at exactly the same
elevation of 1050 m a.s.l. as the Sulawesi plots) was only
2.8 Mg ha1 yr1 (Moser et al., unpublished) and therefore showed
a markedly lower value than the paleotropical forests. In contrast,
leaf production (estimated by leaf litter fall) accounted for only 39%
of the total above-ground production in the Mt Kinabalu dipterocarp
forests, while it was 49% in the Sulawesi forests and reached as much
as 54% in the Ecuadorian pre-montane forest. We conclude from
these ndings that above-ground biomass production of premontane forests on Sulawesi is between the production of
paleotropical dipterocarp forests and neotropical Andean forests.
The below-ground components of trees, in particular the ne
roots, do play a prominent role in productivity while it is negligible
for biomass (Keyes and Grier, 1981; Ruess et al., 1996; Vogt et al.,
1996; Xiao et al., 2003). In our study, ne root production based on
the ingrowth core approach was estimated to be 2.1 Mg ha1 yr1
(which is equivalent to 0.9 Mg carbon ha1 yr1). This appears to
be a rather low value compared with the ranges of 1.1
6.2 Mg ha1 yr1 or 1.215.4 Mg ha1 yr1 given by Vogt et al.
(1996) and Nadelhoffer and Raich (1992) for tropical forests
globally. In their review on ne root biomass and production of
tropical moist forests, Hertel and Leuschner (in press) did not nd
any signicant difference between neotropical lowland (<400 m
a.s.l.) and lower montane (4002000 m a.s.l.) forests. When
applying the above-mentioned criterion for the selection of studies
in pre-montane tropical moist forests to this data base, we
calculated a mean annual ne root production of 4.9 Mg ha1 yr1
for pre-montane forests in the Neotropics and a very similar
amount of 4.1 Mg ha1 yr1 for pre-montane forests in the

Please cite this article in press as: Hertel, D., et al., Below- and above-ground biomass and net primary production in a paleotropical
natural forest (Sulawesi, Indonesia) as compared to neotropical forests. Forest Ecol. Manage. (2009), doi:10.1016/j.foreco.2009.07.019

G Model

FORECO-11765; No of Pages 9
D. Hertel et al. / Forest Ecology and Management xxx (2009) xxxxxx

Paleotropics (Table 6). However, we have to note that all entries in

the paleotropical data set were obtained from studies in the
Hawaiian island forests except of two values that originated from
forests in India. Therefore, the calculated mean value might not be
very representative for the Paleotropics. A more detailed analysis
of the characteristics of southeast Asian rain forest ecosystems in
terms of below-ground productivity, on the other hand, is
prevented by the fact that we do not know of any other study
that investigated ne root production in Malesian forests in the
pre-montane elevational zone. It appears that only one other study
on ne root dynamics in Malesian forests is available from the
lowlands (200 m a.s.l.) of Borneo (Green et al., 2005). Although the
authors do not provide explicit data on annual ne root production,
one can estimate from their data 0.8 Mg ha1 yr1 of ne root
production in the upper 15 cm of the soil, which also represents a
rather low value compared to results of other studies. However, it
remains speculative whether the relatively low ne root production value estimated by the ingrowth core approach in our study is
representative for southeast Asian pre-montane forests. This is all
the more questionable since an earlier study in a pre-montane
forest close to our Sulawesi study plots showed signicant
differences in ne root production estimates depending on the
applied method: while an ingrowth core experiment in the upper
soil showed an annual ne root production similar to our recent
forest plots (c. 2.6 Mg ha1 yr1, Leuschner et al., 2009), a
sequential soil coring approach (combined with a minimum
maximum calculation procedure) resulted in 3.5 Mg ha1 yr1 of
annual ne root production in the upper soil of the same stands
and added up to as much as 5.5 Mg ha1 yr1 in the soil prole
(Harteveld et al., 2007). Hence, more investigations on ne root
dynamics using complementary methods in southeast Asian rain
forests are needed to overcome this uncertainty in ne root
production estimates.
5. Conclusion
The investigation of pre-montane forest plots on Sulawesi,
Indonesia, indicated that these forest ecosystems appear to have a
rather supercial root system in terms of both the ne and the
coarse root biomass. The ratio of below- to above-ground biomass
was relatively low in these forest stands. Moreover, below-ground
net primary production estimated for the rst time for southeast
Asian pre-montane tropical moist forests was also low when
compared with other pre-montane tropical forests in the
Neotropics and the Paleotropics. On the other hand, comparison
of the above-ground biomass stocks and net primary production of
the Sulawesi forest plots with literature data give evidence that the
pre-montane forest on Sulawesi, rich in trees of the Fagaceae, have
higher biomass stocks and productivity compared to neotropical
forests in this elevational zone. However, above-ground biomass
and net primary production were markedly lower than of
dipterocarp pre-montane forests of Malesia. Presumably, the
absence of members of the Dipterocarpaceae in the Sulawesi
forests plots was the reason for their intermediate position in
terms of above-ground stand biomass and production comparing
neotropical and paleotropical pre-montane rain forests. Our study
clearly indicates that it is important to consider possible
differences in the carbon pools in terms of biomass stocks and
productivity of forests of biogeographically different regions for
evaluating the role of tropical moist forests in the global carbon
cycle.
Acknowledgments
This study is part of the German-Indonesian collaborative
research project STORMA (Sonderforschungsbereich 552: Stability

of Rain Forest Margins in Indonesia, subproject C4) funded by the

German Research Foundation (DFG). The nancial support is
gratefully acknowledged. We thank the inhabitants of Toro village
for their hospitality, our local aides for their support during the
eldwork, Beate Michalzik and Daniela Leitner for providing data
on soil chemical properties, and the Indonesian Research Foundation LIPI and the authorities of the Lore Lindu National Park for the
research permission.

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