J. Ecol. Environ. 38(1): 75-84, 2015 75 pISSN : 2287-8327 eISSN : 2288-1220 JOURNAL OF ECOLOGY AND ENVIRONMENT http://www.jecoenv.org Copyright © 2015 The Ecological Society of Korea. All rights are reserved. Carbon stocks and its variations with topography in an intact lowland mixed dipterocarp forest in Brunei Sohye Lee1, Dongho Lee1, Tae Kyung Yoon2, Kamariah Abu Salim3, Saerom Han1, Hyeon Min Yun1, Mihae Yoon1, Eunji Kim1, Woo-Kyun Lee1, Stuart James Davies4 and Yowhan Son1,5,* 1Department of Environmental Science and Ecological Engineering, Korea University, Seoul 136-713, Korea 2Department of Environmental Science and Engineering, Ewha Womans University, Seoul 120-750, Korea 3Environmental and Life Sciences, Faculty of Science, Universiti Brunei Darussalam, Bandar Seri Begawan BE 1410, Brunei 4Centre for Tropical Forest Science, Smithsonian Tropical Research Institute, Washington DC 20013-7012, USA 5Department of Biological of Environmental Science, Qatar University, 2713 Doha, Qatar Abstract Tropical forests play a critical role in mitigating climate change, and therefore, an accurate and precise estimation of trop- ical forest carbon (C) is needed. However, there are many uncertainties associated with C stock estimation in a tropical forest, mainly due to its large variations in biomass. Hence, we quantified C stocks in an intact lowland mixed dipterocarp forest (MDF) in Brunei, and investigated variations in biomass and topography. Tree, deadwood, and soil C stocks were estimated by using the allometric equation method, the line intersect method, and the sampling method, respectively. Understory vegetation and litter were also sampled. We then analyzed spatial variations in tree and deadwood biomass in relation to topography. The total C stock was 321.4 Mg C ha-1, and living biomass, dead organic matter, and soil C stocks accounted for 67%, 11%, and 23%, respectively, of the total. The results reveal that there was a relatively high C stock, even compared to other tropical forests, and that there was no significant relationship between biomass and topography. Our results provide useful reference data and a greater understanding of biomass variations in lowland MDFs, which could be used for greenhouse gas emission-reduction projects. Key words: biomass, carbon pool, carbon stocks, lowland mixed dipterocarp forest, tropical forest, topography INTRODUCTION As international concerns over climate change have increased, there has been rising interest in forests, which sequester more carbon (C) than any other terrestrial eco- system (Gibbs et al. 2007). Any forest-based project that aims to mitigate climate change requires an accurate and precise estimation of forest C (Ravindranath and Ostwald 2008). Further research on tropical forest C stock estima- tion is needed for the following reasons: firstly, tropical forests have a great potential for sequestrating carbon di- oxide from the atmosphere because they have the highest primary productivity and occupy the largest area of all of the global forests (Pan et al. 2011); secondly, more refer- ence data are needed to lower the uncertainty when es- timating tropical forest C stocks because complex stand structures and high species diversity make the estimation prone to many errors (Chave et al. 2004); and lastly, 15- 20% of global greenhouse gas emissions are caused by C emitted into the atmosphere by tropical deforestation Received 04 January 2015, Accepted 09 January 2015 *Corresponding Author E-mail: yson@korea.ac.kr Tel: +82-2-3290-3015 http://dx.doi.org/10.5141/ecoenv.2015.008 Research Paper This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Licens (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. J. Ecol. Environ. 38(1): 75-84, 2015 http://dx.doi.org/10.5141/ecoenv.2015.008 76 biomass for that geographical region (Houghton 2005, de Castilho et al. 2006). Consequently, it is essential to take into account several environmental factors when describ- ing biomass variations. Tropical forests exhibit large spa- tial variability in tree biomass (Laurance et al. 1999, Chave et al. 2001, 2003); however, this variation is poorly under- stood (Houghton 2005). Therefore, investigating the ef- fects of topography on variations in biomass is necessary to understand the forest in large-scale. This study aimed to achieve the following objectives: 1) to provide reference data for estimating C stocks of an in- tact lowland MDF in Brunei; and 2) to investigate the rela- tionship between biomass (aboveground and deadwood) and topographical factors. This is the first study that has estimated forest C stocks in Brunei and recorded not only the generally reported aboveground biomass (AGB) but also the total biomass in a forest ecosystem. MATERIALS AND METHODS Study site The study was conducted in the undisturbed Kuala Belalong lowland MDF, which is part of the Ulu Tembu- long National Park, Brunei Darussalam (04°63′50.3″ N, 115°22′79.1″ E) (Fig. 1a). Meteorological data that were col- lected from 2006 to 2010 at Semabat Agricultural Station, which is located 9 km northwest of Kuala Belalong, show that the temperature is slightly variable, with monthly mean maxima of between 31.1°C (July 2010) and 34.2°C (May 2007) and minima around 26°C. The mean annual precipitation is approximately 4,582 mm, with no distinct dry season. The soils are yellow or red and are mainly in- ceptisols and ultisols derived from shale parent materi- als (Ashton and Hall 1992), according to the United States Soil Survey Classification. A detailed description of the local climate, topography, soil, and hydrology is provided by Cranbrook and Edwards (1994). The canopy consists of the crowns of the biggest trees at 30-40 m above the ground, which are only surpassed in height by emergents that are over 60 m tall (Poulsen et al. 1996). The domi- nant canopy family is Dipterocarpaceae, with individuals of the genera Shorea (Dipterocarpaceae), Dryobalanops (Dipterocarpaceae), and Koompassia (Caesalpiniaceae) being the main emergents (Ashton and Hall 1992). Small et al. (2004) found 1,062 stems (diameter at breast height (DBH) ≥ 5 cm) and 278 species, representing 110 genera in 49 families, in a 1-ha quadrat (1 ha = 104 m2) in this area. (Gibbs et al. 2007); therefore, greenhouse gas emission- reduction projects must be given priority. However, there have been few studies conducted on the estimation of tropical forest C stocks, because tropical forests are gen- erally located in developing countries, in which adequate research funding is difficult to obtain (Malhi et al. 2009), particularly in Southeast Asia (Pan et al. 2011). One of the typical forest types in Southeast Asia is mixed dipterocarp forest (MDF). The Dipterocarpaceae is a family of tall and fast-growing trees that dominate the upper canopy of tropical forests. These vegetation zones are called MDFs due to their overwhelming presence (Ap- panah and Turnbull 1998). This family plays an impor- tant role in the timber market of many Southeast Asian countries because of their excellent quality (Poore 1989). It has been documented that the floristic compositions and canopy structures of MDFs vary with precipitation, topography, and soil nutrients (Ashton and Hall 1992, Appanah and Turnbull 1998). In addition, the biomass in MDFs exhibits high variance (e.g., 271 ± 19 to 478 ± 38 Mg ha-1) (Laumonier et al. 2010). Consequently, in order to decrease uncertainty in C stock estimation in MDFs, ob- taining reference data is essential. Kuala Belalong lowland MDF (i.e., this study area) has been protected by the Bruneian government; conse- quently, there are no records of significant disturbances, either natural or artificial (Cranbrook and Edwards 1994). Therefore, it is a completely intact primary forest. This is important, as many forests in developing countries that have been destroyed were tropical forests, and it is very difficult to find completely intact tropical forests for re- search purposes. For greenhouse gas emission-reduction projects, studies conducted in intact tropical forests can provide important data. In addition, the study area was established as the part of the Center for Tropical Forest Science (CTFS) project, which is a global network of for- est researchers (http://www.ctfs.si.edu). Over 60 forest re- search plots in the Americas, Africa, Asia, and Europe are included in long-term research using the same methodol- ogy, for easy data sharing. Therefore, the scientific value of this study area can be considered very high. There have been approximately 260 papers published concerning Kuala Belalong lowland MDF, on various subjects: biodi- versity, soil, forest structure, biogeography, etc. However, this is the first study that has investigated C stocks. Knowing spatial variations in forest biomass is also important because carbon dioxide emissions from de- forestation are determined by the original biomass of the forest that was destroyed, not necessarily by the average Carbon stocks in an intact lowland mixed dipterocarp forest 77 http://w w w.jecoenv.org MDF in East Kalimantan, Indonesia (Basuki et al. 2009): ln(AGB) = – 0.744 + 2.188ln(DBH) + ln(WD), (1) where AGB is in kg tree-1, DBH is in cm, WD (wood den- sity) is in g cm-3, and the correction factor is 1.047 (Sprugel 1983). A WD value of 0.6 g cm-3 was found in a previous study conducted in this area (Osunkoya et al. 2007). The belowground biomass (BGB) was estimated using a BGB- AGB ratio of 0.18, obtained from the Pasoh Forest Reserve, Malaysia (Niiyama et al. 2010). Understory vegetation (trees with a DBH < 1 cm and herbs) biomass was estimated using the harvest method (Ravindranath and Ostwald 2008) within 2 × 2 m quadrats, which were randomly established in each 60 × 60 m quad- rat (n = 6). All of the collected samples were oven-dried at 70°C and weighed using an electronic scale. To convert living biomass into C stocks, we assumed that 50% of the dry mass was C, based on the results from a study in Malaysia that had a similar species composi- tion (Kenzo et al. 2010). Experimental design The study was conducted in six 60 × 60 m quadrats, separated by a distance of approximately 100 m at an ele- vation of between 200 and 300 m above sea level (Fig. 1b). For ease of identification, numbered poles were placed every 10 m in both directions (rows and columns), and the 10 m was measured as a linear distance that accounted for the gradient. The 60 × 60 m quadrats were divided into several sub-quadrats (Fig. 1c). Large forest plots, includ- ing the CTFS plots, were established using this design, and they share the same methods of mapping and cen- susing trees. A detailed description of quadrat establish- ment and tree measurement is given by Condit (1998). Living biomass and C stock estimation The AGB (DBH ≥ 1 cm) was estimated by using the bio- mass estimation equation approach (Ravindranath and Ostwald 2008). DBH data were acquired from the six 60 × 60 m quadrats. We selected the following biomass estima- tion equation which was developed in a tropical lowland Fig. 1. The location of Brunei Darussalam (a), six quadrats (60 × 60 m) in Kuala Belalong lowland mixed dipterocarp forest, where the study was conducted (b), and the experimental design of each 60 × 60 m quadrant (c). 0 60 120 240 360 480 (m) Elevation (m) 60 m N S W E High : 307 Low : 46 a cb J. Ecol. Environ. 38(1): 75-84, 2015 http://dx.doi.org/10.5141/ecoenv.2015.008 78 cm long cylindrical metal corer (406.94 cm3) at three ran- dom points in each six 60 × 60 m quadrat (n = 18). The samples were then air dried and sieved through a 2-mm mesh screen (US standard No. 10) for determining bulk density and concentrations of C. Soil bulk density was de- termined by dividing the weight of soil samples dried at 105°C by the volume of the metal corer. An elemental an- alyzer (vario Macro cube CN, Elementar, Germany) was used to measure the soil C concentration. Soil C stocks at each depth were calculated from the soil C concentration and the bulk density of each soil sample. Variations in living and dead wood biomass in terms of topographical characteristics To analyze variations in biomass and topographical characteristics, each 60 × 60 m quadrat was divided into nine 20 × 20 m sub-quadrats. The biomass and topogra- phy were analyzed using PROC MEANS, PROC CORR, and PROC REG in SAS 9.3 software (SAS Institute Inc., Cary, NC, USA). Topographical data were obtained from LiDAR and ArcGIS. RESULTS AND DISCUSSION Living biomass Total AGB was estimated as 361.8 ± 21.0 Mg ha-1 (Table 1), which was classified as in the highest biomass class category (AGB > 350 Mg ha-1) according to the classifica- tion criteria proposed by Saatchi et al. (2011). Only 7% in Asia, 8.7% in Africa, and 7.4% in Latin America has more than 350 Mg ha-1 AGB (Saatchi et al. 2011). However, this value is much lower than that recorded in the Lambir Hills National Park, Sarawak, Malaysia (544.8 Mg ha-1; Kataya- ma et al. 2013), which has a similar primary MDF near our study site. There could be several reasons for this: 1) the dominant tree height differs between areas. The canopy of our site was approximately 30 to 40 m in height, and the density of tall trees was not high, whereas Lambir National Park has a continuous 40 to 50 m tree layer (Katayama et al. 2013); 2) the result obtained in Lambir included lianas. In a lowland rainforest in Venezuela, the mean biomass of a liana with a 10-cm DBH is nearly four times the leaf biomass of a 10-cm DBH tree (Putz and Chai 1987). There- fore, lianas might be an important component in estimat- ing the biomass of tropical forests; 3) lastly, environmen- tal conditions are different. The mean annual rainfall in Lambir (2600 mm) is much lower than that at our site, the Dead organic matter biomass and C stock esti- mation Deadwood biomass was calculated as the sum of log (fallen dead wood with diameter ≥ 10 cm) and snag (standing deadwood with DBH ≥ 10 cm) biomass. The log biomass was estimated using the line intersect method (Marshall et al. 2000), which is as follows: Blog = WDlog × Vlog (2) Vlog = π2/8LΣ di2 cosλi n i=1 (3) where Blog is the log biomass (Mg ha-1), WDlog is the log WD (g m-3), Vlog is the log volume (m3 ha-1), L is the length of the line transect (m), n is the number of log pieces that intersects the line transect, di is the diameter (≥10 cm) of log i at the point of intersection (cm), and λi is the angle from the horizontal of the log (n = i) crossed by the line transect (degrees). To estimate the Vlog, six 60 m transect lines were established in each 60 × 60 m quadrat at regu- lar intervals. The di and λi were measured along each tran- sect line. To estimate WDlog, all the logs were subsampled in a 20 × 20 m sub-quadrat of each 60 × 60 m quadrat (n = 6). The volumes of the samples were determined using the ethanol displacement method (Saner et al. 2012). The samples were then dried in an oven to a constant weight (70°C) and weighed using an electronic scale. The snag biomass (Bsnag) was the product of the WD (WDsnag) and the volume of snag (Vsnag). Due to a lack of data for the WDsnag, the same value of the WDlog was ap- plied to the WDsnag. To estimate the Vsnag, DBH, height, and snag structure (stem only or stem plus branches) were re- corded for all snags in the same six 60 × 60 m quadrats. Snag height was visually estimated, and tree Vsnag was cal- culated following the methods described in Gale (2000). The Bsnag was estimated by multiplying the Vsnag and the WDlog. To convert dead organic matter biomass into C stocks, we assumed that 50% of the dry mass was C. Litter (twigs, leaves, and reproductive organs) biomass was also sampled within 2 × 2 m quadrats, which were randomly established in each 60 × 60 m quadrat (n = 6). All of the collected samples were oven-dried at 70°C and weighed using an electronic scale. Estimation of soil organic C Soil was sampled in August and December 2013 at 0 to 10 cm, 10 to 20 cm, and 20 to 30 cm depths using a 10- Carbon stocks in an intact lowland mixed dipterocarp forest 79 http://w w w.jecoenv.org MDF was used for the estimation (Niiyama et al. 2010), the resulting BGB was 120.9 Mg ha-1. According to this result, the BGB-AGB ratio is estimated as 0.33, while val- ues from previous studies conducted in other tropical forests were 0.14 (Chave et al. 2005), 0.19 (Jackson et al. 1996), and ≤0.24 (Cairns et al. 1997). Compared to these reported values, a ratio of 0.33 might be considered an overestimation. In fact, the Malaysian study area where the DBH-BGB regression equation was developed has a DBH distribution that is different from that in our study area, and the area is dominated by trees with a large DBH. In addition, Brown (2002) reported that tree age was also an important factor that had to be considered when us- ing a BGB regression equation. Root biomass also differs among tropical forests, and depends on meteorological and soil characteristics (Brown and Lugo 1982, Sanford and Cuevas 1996). For these reasons, using the above DBH-BGB regression equation in our study area may not have been ideal. The biomass of woody plants (≤1 cm DBH) and herbs was 0.2 ± 0.1 Mg ha-1, and this was relatively low compared to the total living biomass (<0.1%). This result is similar to that found in a previous study (Brown 1997); biomass allocation in woody plants is a typical characteristic of mature tropical forests, and understory vegetation plays important ecological roles in tropical forests. Indeed, the rate of forest tree development is higher in areas without understory cover (Parrotta 1995). Therefore, understory vegetation may have the same value as other C pools in tropical forest restoration, even though its biomass allo- cation is small (Lamb 1998). soil has a higher sand content (62 to 72%), and the range of elevation (20 to 470 m) is greater (Katayama et al. 2013). Consequently, the AGB depends on the area, even in the same MDF, for many reasons. The specialized estimation for a particular area might be required in this case. The stand density of the study site was 6718.1 ± 328.5 stems ha-1 (mean ± SE), and about half (48.1%) of the AGB was in trees with a DBH greater than 50 cm, which ac- counted for 0.6% of the total number of stems. The AGB of the trees with a DBH of 1.0 to 9.9 cm (that accounted for 91% of the total number of stems) accounted for 8.1% of the total AGB (Table 1). This suggests that the study site is a climax forest and has a large number of highly com- petitive young trees, and only a small number of big trees survive (Alder and Synnott 1992). In addition, the site has an uneven topography and an easily disaggregated soil type, which results in severe soil erosion (Cranbrook and Edwards 1994); this also might inhibit the growth of large trees. Generally, trees with a DBH of less than 10 cm are usually disregarded in AGB estimations. In this study, however, the AGB of trees with a DBH of 1.0 to 9.9 cm was also estimated, and the result (8.1% of the total AGB) was not negligible. As a result, to enhance the accuracy and precision of AGB estimations in intact tropical forests with a similar DBH profile as this area, the inclusion of trees with a DBH lower than 10 cm is essential. The total basal area of the study site was 38.8 m2 ha-1, which is similar to that of a previous study conducted in an undisturbed Ma- laysian lowland MDF (34.5 m2 ha-1; Sato et al. 2013). The BGB of the study site was estimated as 65.1 Mg ha-1, using a BGB-AGB ratio of 0.18. When the DBH-BGB regression equation developed in a Malaysian lowland Table 1. Estimates of number of stems, basal area (BA), and aboveground biomass (AGB) in Kuala Belalong lowland mixed dipterocarp forest DBH class (cm) No. of stems (ha-1) BA (m2 ha-1) AGB (Mg ha-1) Mean SE % of total Mean SE % of total Mean SE % of total 1.0-9.9 6113.9 320.1 91.0 5.3 0.2 11.9 29.2 1.2 8.1 10.0-19.9 360.2 17.9 5.4 5.4 0.3 12.2 36.7 1.9 10.1 20.0-29.9 116.2 6.2 1.7 5.4 0.3 12.3 41.0 2.2 11.3 30.0-39.9 58.8 4.4 0.9 5.5 0.4 12.5 44.7 3.0 12.4 40.0-49.9 27.8 3.1 0.4 4.3 0.5 9.7 36.0 4.3 10.0 50.0-59.9 15.3 2.7 0.2 3.6 0.6 8.1 31.3 5.6 8.7 60.0-69.9 10.2 3.0 0.2 3.3 1.0 7.4 29.7 9.2 8.2 70.0-79.9 3.2 0.5 0.0 1.5 0.3 3.3 13.6 2.4 3.8 80.0-89.9 5.6 2.3 0.1 3.1 1.3 7.1 29.9 12.2 8.3 90.0-99.9 2.3 1.3 0.0 1.6 0.9 3.7 16.1 9.0 4.4 ≥100.0 4.6 0.9 0.1 5.2 1.4 11.8 53.5 14.8 14.8 Total 6718.1 328.5 100.0 44.1 2.1 100.0 361.8 21.0 100.0 DBH, diameter at breast height; SE, standard error. J. Ecol. Environ. 38(1): 75-84, 2015 http://dx.doi.org/10.5141/ecoenv.2015.008 80 However, our study site had little seasonal variation, and monthly litterfall was relatively constant, therefore, the litter from standing crops in this area might exhibit little temporal variation. Soil C stocks The total soil C stocks between 0 and 30 cm in depth was estimated as 74.2 Mg C ha-1, 46.5% of which was be- tween 0 to 10 cm, 28.7% was between 10 to 20 cm, and 24.8% was between 20 to 30 cm. The soil C concentration (g kg-1) of 0-10, 10-20, 20-30 cm depths were 38.4, 19.4, 14.2, respectively, decreasing from 0 to 30 cm. Because of frequent rain, uneven topography, and a silty clay soil type, the soil of the study site is relatively shallow, and is rarely deeper than 2 m (Cranbrook and Edwards 1994). In addition, there were many roots and stones present on the soil surface, making core sampling difficult. In a previous study conducted in a primary tropical forest in Singapore (Ngo et al. 2013), the soil was 3 m deep, and soil C stocks between 0 and 300 cm in depth were estimated as 132.5 Mg C ha-1. Variations in soil characteristics with- in our study area suggest that the optimal investigative method should be specialized for the target area (Carter 1993). Because soil C accounts for the second-largest pro- portion of the total C stock, accurate and precise soil C estimation is important. Dead organic matter The volume of dead wood in the study site was esti- mated as 122.3 ± 25.7 m3 ha-1, and this value is similar to that obtained in a previous study (116 m3 ha-1; Yoneda et al. 1990) in the MDF of Sumatra island (Table 2). Log vol- ume was 103.4 ± 24.5 m3 ha- 1, and it accounted for 84.5% of the entire dead wood volume. This value is 57% higher than that obtained in a previous study conducted in the same area (66.0 ± 10.2 m3 ha-1; Gale 2000). The difference in the two results might be due to the facts that: 1) the cur- rent study included logs with a DBH of 10 to 20 cm; and 2) transect lines were established mainly on ridges. Gale (2000) found that log volume tended to decrease from the ridge to the valley. In this study, snag volume accounted for 15.5% of the entire dead wood volume (18.9 ± 10.8 m3 ha-1), and this was lower than that of the previous study (37.7 ± 4.7 m3 ha-1; Gale 2000). The log WD was 0.50 ± 0.04 g cm-3 (n = 36), which is identical to the result of a previous study conducted in a Venezuelan tropical rain forest (0.5 g cm-3; Delaney et al. 1998). Log and snag dry weights were estimated by multiplying the WD with the volume. The total biomass of dead wood was estimated as 61.2 ± 12.9 Mg ha-1. In an old forest, such as in our study area, the inputs and outputs of dead wood are theoretically in balance, and dead wood biomass is relatively constant (Harmon and Sexton 1996). Therefore, it can be assumed that the total dead wood biomass would remain constant, as the study site was an old forest. Our results should be highly accurate, as the study areas (six of 60 × 60 m quad- rats) were large in comparison with those in other studies, e. g., 50 × 50 m by Delaney et al. (1998); 30 × 40 m, Tori- yama et al. (2014). The amount of dead wood in tropical forests has been poorly quantified, but is extremely vari- able (it can account for less than 10% to more than 40% of the total biomass; Brown 1997), and depends on various factors. Therefore, the current study’s results should be highly accurate and could provide useful reference data for intact tropical MDFs. The litter dry weight was estimated as 6.2 ± 1.0 Mg ha-1, which was 10% of the dry weight of dead wood. Twig dry weight accounted for 59.7% of the total litter, and leaves accounted for 40.1%. Almost all of the litter was composed of twigs and leaves, and the dry weight of the reproductive organs was relatively insignificant. Litter dry weight was very similar to that found in a previous study: 5.75 Mg ha-1 in a MDF in the Andulau Forest Reserve, Brunei (Moran et al. 2000). Patterns of litter from standing crops usually ex- hibit temporal variations (e.g., seasons), and tropical for- ests are not an exception (3.0 to 10.5 Mg ha-1; Spain 1984). Table 2. Estimated volume (m3 ha-1) and dry weight (Mg ha-1) of log and snag in Kuala Belalong lowland mixed dipterocarp forest Volume (m3 ha-1) Dry weight (Mg ha-1) Mean SE % of total Mean SE Log 103.4 24.5 84.5 51.7 12.3 Snag 18.9 10.8 15.5 9.5 5.4 Total 122.3 25.7 100.0 61.2 12.9 SE, standard error. Tabl e 3 . Estimates of carbon (C) stocks in each C pool (Mg C ha-1) in Kuala Belalong lowland mixed dipterocarp forest Carbon pools Mg C ha-1 % of total Living biomass 213.6 66.5 Aboveground tree biomass (DBH ≥ 1 cm) 180.9 56.3 Belowground tree biomass (DBH ≥ 1 cm) 32.6 10.1 Woody plant (DBH < 1 cm) and herb biomass 0.1 0.0 Dead organic matter 33.6 10.5 Log 25.8 8.0 Snag 4.7 1.5 Litter 3.1 1.0 Soil (to 30 cm) 74.2 23.0 0-30 cm 74.2 23.0 Total 321.4 100.0 DBH, diameter at breast height. Carbon stocks in an intact lowland mixed dipterocarp forest 81 http://w w w.jecoenv.org Variations in living biomass and dead wood biomass associated with topographical charac- teristics Variations in biomass and topography among the 20 × 20 m quadrats (n = 54) varied widely (Fig. 2). The total liv- ing biomass varied from 108.3 to 1509.8 Mg ha-1, which was highly variable compared to the results from a previ- ous study (189.8 to 422.8 Mg ha-1; de Castilho et al. 2006). Dead wood biomass was also variable (0 to 321.7 Mg ha- 1), and the coefficients of variation (CVs) of aboveground tree biomass, belowground tree biomass, log dead wood, and snag dead wood were 176.8%, 81.4%, 67.4%, and 37.1%, respectively. Aspect and elevation varied between Total C stocks and allocation The C stocks and allocation to each C pool are shown in Table 3. The total C stock was estimated as 321.4 Mg C ha-1. This value is higher than that found in the Bukit Ti- mah National Park, Singapore, which has a similar stand structure (337 Mg C ha-1; Ngo et al. 2013). The C stocks of the living biomass, the dead organic matter, and the soil accounted for 67%, 11%, and 23%, respectively, of the to- tal. This suggests that living biomass accounts for a high proportion of C, whereas that by dead organic matter and soil is low. This is typical of tropical rain forests with high primary productivities and decomposition rates (Pan et al. 2011). Fi g . 2. Variations in aboveground tree biomass (AB), belowground tree biomass (BB), all living biomass (LB), log, snag, all dead wood biomass (DW), aspect, elevation, and slope. Numbers on the upper panels are correlation coefficients (P > 0.05). The diagonal cells show histograms. Curves on the lower panels are weighted scatterplots. J. Ecol. Environ. 38(1): 75-84, 2015 http://dx.doi.org/10.5141/ecoenv.2015.008 82 C ha-1. Living biomass, dead organic matter, and soil ac- counted for 67%, 11%, and 23%, respectively, of the total C stock. One of the remarkable characteristics of this forest is that it is dominated by small trees. Variations in living and dead wood biomasses were high; however, there were no significant relationships between biomass and topo- graphical factors. Our results provide useful reference data and background information for understanding the biomass variations specialized in lowland MDFs. ACKNOWLEDGMENTS This work was supported by research grants from the Korea Forest Service under the project title “Developing Techniques on Detection and Quantification of Forest Carbon to Secure Forest Resources in Intact Rainforests” (2013-2016). We would like to thank the University of Brunei Darussalam for allowing us to conduct the study at Kuala Belalong, Kuala Belalong Forest Science Center staff for their support, Heart of Boreo, and the Ministry of Primary Resources for granting us export permits. LITERATURE CITED Alder D, Synnott TJ. 1992. Permanent Sample Plot Tech- niques for Mixed Tropical Forest. Oxford Forestry Insti- tute and University of Oxford, Oxford. Appanah S, Turnbull JM. 1998. A Review of Dipterocarps: Taxonomy, Ecology, and Silviculture. Center for Inter- national Forestry Research, Bogor. Ashton PS, Hall P. 1992. Comparisons of structure among mixed dipterocarp forests of north-western Borneo. J Ecol 90: 459-481. Basuki TM, van Laake PE, Skidmore AK, Hussin YA. 2009. Allometric equations for estimating the above-ground biomass in tropical lowland Dipterocarp forests. For Ecol Manag 257: 1684-1694. Brown S. 1997. Estimating Biomass and Biomass Change of Tropical Forests: A Primer, Vol. 134. Food and Agricul- ture Organization, Rome. Brown S. 2002. Measuring carbon in forests: current status and future challenges. Environ Pollut 116: 363-372. Brown S, Lugo AE. 1982. The storage and production of or- ganic matter in tropical forests and their role in the glob- al carbon cycle. Biotropica 14:161-187. Cairns MA, Brown S, Helmer EH, Baumgardner GA. 1997. Root biomass allocation in the world’s upland forests. Oecologia 111: 1-11. 35.3° and 303°, and 161.5 to 262.5 m, respectively, and the slope ranged from 17.3° to 46°. No statistically significant correlations were found be- tween biomass and topographical factors (Fig. 2), and only weak, non-significant correlation was found be- tween log biomass and slope (r = 0.2; P = 0.1). There are several possible reasons for this result: 1) there was no evi- dence of spatial variations in tree growth or mortality in our study site. In fact, the tree growth rate in the study site (3.3 ± 0.14 mm yr-1) and the mortality rate—estimated as the ratio of dead wood to living tree biomass (0.1 ± 0.02)— were relatively constant, regardless of the topography. This is similar to that found in previous studies conducted in central Amazonia and Borneo (de Castilho et al. 2006, Osunkoya et al. 2007), and suggests that topography has no effect on growth and survival; 2) there may have been a possibility of topographical variation within the 20 × 20 m quadrats. In our study, the biomass and topographi- cal data were analyzed as 20 × 20 m quadrat units, and in the process of producing an average for each quadrat, the variation inside each quadrat could have been missed; 3) the key factors that determine biomass variation might not have been included in this study. In many tropical forests, light is critical for tree growth and survival (King 1991, Schnitzer et al. 2005). Although other resources, such as water and nutrients, in tropical forests are usually easily available to trees, light is highly limited. There was no evidence of a relationship between canopy openness and topography in our study site. In fact, the distribution of DBH classes did not exhibit any spatial variation, sug- gesting that competition for light was uniform through- out the study area; 4) the result may be related to tropi- cal forest complexity. Topography generally covaries with many other variables, such as soil type, canopy openness, and soil water availability, and it can also affect forest dy- namics and nutrient cycling (de Castilho et al. 2006). It is probable that topography alone does not affect variations in biomass. However, many environmental factors closely related to biomass are affected by topography. In respect to forest dynamics, the high spatial variance in biomass suggests that forest dynamics may differ, depending on the topography. This could lead to significant differences in C fluxes, even though biomass is not directly affected by topography (Clark and Clark 2000). CONCLUSION Our study quantified the C stock of the Kuala Belalong lowland MDF, Brunei Darussalam, which was 321.4 Mg Carbon stocks in an intact lowland mixed dipterocarp forest 83 http://w w w.jecoenv.org DC, pp 13-21. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. 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