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Ecosystem carbon stock of a tropical mangrove forest in North Sulawesi, Indonesia
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Shunyang CHEN1, Bin CHEN1, Pramudji SASTROSUWONDO2, I Wayan Eka DHARMAWAN2, 3, Danyun OU1, Xijie YIN1, Weiwei YU1, Guangcheng CHEN1, *
Acta Oceanologica Sinica | 2018, 37(12) : 85 - 91
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Acta Oceanologica Sinica | 2018, 37(12): 85-91
• Coastal Environment and Biodiversity in North Sulawesi, Indonesia •
Ecosystem carbon stock of a tropical mangrove forest in North Sulawesi, Indonesia
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Shunyang CHEN1, Bin CHEN1, Pramudji SASTROSUWONDO2, I Wayan Eka DHARMAWAN2, 3, Danyun OU1, Xijie YIN1, Weiwei YU1, Guangcheng CHEN1, *
Affiliations
  • 1 Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
  • 2 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia
  • 3 Technical Implementing Unit Marine Life Conservation Biak, Indonesian Institute of Sciences, Biak 98152, Indonesia
Published: 2018-12-25 doi: 10.1007/s13131-018-1290-5
Outline
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Recent studies have highlighted the valuable role played by mangrove forests in carbon sequestration and storage. Although Indonesia accounts for a large proportion of global mangrove area, knowledge on the carbon stock and sources in the Indonesian mangrove is still limited. In this study, we quantified the ecosystem organic carbon (OC) stock and its spatial variation at an oceanic mangrove in Wori, North Sulawesi, Indonesia. The sources of soil OC were also investigated. The results showed that the mangrove soil had a substantial OC stock containing 15.4 kg/m2 (calculated by carbon) in the top 50 cm soil, and represented the majority of the ecosystem OC stock at the Wori mangrove. The mangrove biomass and ecosystem OC stock were 8.3 kg/m2 and 23.7 kg/m2, respectively. There was no significantly difference in the soil OC stock among the stations with difference distances offshore, while the highest mangrove biomass OC stock was found at the seaward station. Isotope mixing calculations showed that the rich OC in mangrove soils was attributed to the accumulated autochthonous mangrove source while the suspended organic matter in tidal water and the mangrove-adjacent seagrass contributed less than 20% to the soil OC. The results further demonstrated the importances of the oceanic mangrove in carbon storage and the mangrove plants in contributing OC to their soils.

mangrove  /  carbon stock  /  biomass  /  soil  /  stable isotopes  /  Indonesia
Shunyang CHEN, Bin CHEN, Pramudji SASTROSUWONDO, I Wayan Eka DHARMAWAN, Danyun OU, Xijie YIN, Weiwei YU, Guangcheng CHEN. Ecosystem carbon stock of a tropical mangrove forest in North Sulawesi, Indonesia[J]. Acta Oceanologica Sinica, 2018 , 37 (12) : 85 -91 . DOI: 10.1007/s13131-018-1290-5
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1 Introduction
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Although mangrove forests occupy only 2% of the world’s coastal ocean area, they account for around 5% of net primary production, 12% of ecosystem respiration and 30% of carbon burial on all continental margins in subtropical and tropical seas (Alongi and Mukhopadhyay, 2015). Recently, numerous studies have highlighted the importance of mangrove ecosystems in carbon stock (Donato et al., 2011; Keith et al., 2009; Alongi, 2014), because the mangrove plants are highly productive (Alongi, 2014) and the anoxic condition in their highly saturated or flooded soils limits the decomposition of organic carbon (OC) in soil (Armentano and Menges, 1986; Alongi, 1998, 2009). Globally, the mangrove ecosystem stores an OC pool three times more than the typical upland tropical forests and the ecosystem OC stocks can even be up to 1 023 Mg/hm2 in certain mangroves (Donato et al., 2011). However, regional assessments of carbon stocks are still limited and should be viewed for the accuracy of global budget, due to the great geographic variation in carbon stock in mangrove wetlands. Such information is also important for the inventory of national greenhouse gases emissions from mangrove wetlands because loss of their carbon stock due to human activities is equivalent to relevant carbon dioxide emission to atmosphere (Hiraishi et al., 2014).
Soil pool is the majority of ecosystem carbon stock in mangroves (Donato et al., 2011; Alongi et al., 2016), and the soil stock accounts for 49%–98% of the ecosystem stock in some tropical mangrove wetlands (Donato et al., 2011). The soil OC comprises the organic matter derived from mangrove, benthic algae, and allochthonous sources including suspended organic matter (SPOM) and adjacent seagrass (Wooller et al., 2003; Kristensen et al., 2008). Although mangrove derived OC generally accounts for the majority of the soil OC in mangrove wetlands (Kristensen et al., 2008), non-mangrove sources could also dominate the OC sources in some mangrove wetlands (Wooller et al., 2003). The source of OC is an important factor determining the soil carbon sequestration because different sources have variable carbon concentrations (Chen et al., 2017); however, sources of OC in mangrove soils have rarely been studied in details.
Indonesia with a total mangrove area of 2.9×106 hm2, has the largest extent of mangroves around the world and accounts for around half the Asian mangrove area (FAO, 2007). Although some studies have suggested that the Indonesian mangrove wetlands are globally significant carbon sink and stock (Donato et al., 2011; Murdiyarso et al., 2015; Alongi et al., 2016), currently only a few studies reported the mangrove ecosystem carbon stocks in Indonesia (Donato et al., 2011; Murdiyarso et al., 2015, Alongi et al., 2016). These data are very limited for the knowledge and accurate estimation of the national mangrove carbon stock in Indonesia. The present study studied the ecosystem carbon stock and its spatial variation pattern with tidal elevation in a North Sulawesi mangrove, and the soil OC sources were also investigated via isotopic analysis.
2 Materials and methods
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2.1 Study area
The present study was conducted at an oceanic mangrove forest in Wori (1°35′44.16′′N, 124°50′48.97′′E), North Sulawesi, Indonesia. The North Sulawesi had a typical equatorial climate, and the mean temperatures at sea level are uniform, varying by only a few degrees throughout the region and throughout the year, from 20°C to 28°C. Tides in this area were mixed and mainly semi-diurnal, and fluctuate slightly with an annual tidal range of 2.4 m. The mangrove forest consisted of Rhizophora apiculata, Avicennia lanata, Bruguiera gymnorrhiza and Sonneratia alba, and seagrass meadow occurred at the seaward fringe of the mangrove forest, which was dominated by Halodule pinifolia, Cymodocea rotundata and Thalassia hemprichii (Chen et al., 2017).
2.2 Vegetation investigation
Three sampling stations were established at the landward (LW), middle zone (MZ) and the seaward (SW) zones at the Wori mangrove. At each station, three 10 m×10 m plots were randomly setup for vegetation investigation. Within each plot, the species and canopy height of all trees and saplings were recorded. Breast height diameters (DBH) of S. alba, A. lanata and B. gymnorrhiza were measured at the height of 1.3 m. DBH of R. apiculata was measured above the highest prop-root when the prop roots were developed over 1.3 m. Senescent mangrove leaves (with a yellowish color) of the dominant species were collected at each sampling station by gently shaking the branches.
The aboveground biomass (AGB) and belowground biomass (BGB) were estimated using the common allometric equations with tree diameter DBH and wood density (ρ) as the independent variables for each tree species.
For R. apiculata, AGB=0.235×DBH2.420; BGB=0.063 9×DBH2.546 (Ong et al., 2004).
For other species: AGB=0.251×ρ×DBH2.460; BGB=0.019 9×ρ0.899×DBH2.220 (Komiyama et al., 2005).
The ρ were 0.699 g/cm3, 0.506 g/cm3 and 0.475 g/cm3 for B. gymnorrhiza, A. lanata and S. alba, respectively (Komiyama et al., 2005).
Total biomass OC stock (BOS) was calculated using the following formula:
$BOS=AGB\times C_ {\rm{AG}}+BGB\times C_ {\rm{BG}},$
where CAG and CBG were the OC proportions of the aboveground biomass and belowground biomass, respectively, and their respective values were 0.47 and 0.39 (Murdiyarso et al., 2015).
2.3 Soil samples collection
Soil samples were collected from each sampling plot using a PVC corer (inner diameter of 7.0 cm) with a cutter at the bottom. The sampling depth was 50 cm at the LW and MZ stations, and was limited to 20 cm at the SW station. The sediment cores were sliced into subsections by 10 cm intervals. Each of these subsections was weighted and then divided into two halves, with one half oven-dried under 60°C to achieve the water content of these fresh samples and estimate the bulk density. Another half was then air-dried for later analysis of soil OC concentration and δ13C after the visible benthic animals, plant residues and stones (>2 mm) were removed.
2.4 Soil and plant samples analyses
The OC and δ13C in soil and plant samples were measured using a Thermo Flash EA 1112 HT-Delta V Advantages system. For isotopic analysis of soils, air-dried subsamples were placed into silver cups, acidified with diluted HCl (5%) and then oven-dried at 40°C to remove the carbonates. Mangrove leaves were not treated with HCl because no carbonate was expected to be present. The stable carbon isotopic composition was reported in the δ notation as the ratio of the heavy to the light stable isotope in the sample (Rsample) relative to that of a standard (Rstandard), i.e., δsample=1 000×[(Rsample/Rstandard)–1], with standard=Vienna Pee Dee Bellemnite (VPDB) and R=13C/12C. The reproducibility of OC and stable isotopic analysis were <0.6% and <0.2‰, respectively.
2.5 Statistical analyses and estimation of soil OC sources
The normality of variables was checked using Kolmogorov–Smirnov test. The results showed that the distribution patterns of all soil parameters were distributed normally (p>0.05), so no transformation of data was performed. The differences in plant biomass and the biomass OC stock among the stations were compared using one-way analysis of variance (ANOVA). Two-way ANOVAs was used to test the differences in soil parameters with the sampling station and soil depth as factors. If the difference was significant (p<0.05), a post-hoc Tukey test was used to determine the difference. All statistical analyses were performed using SPSS 17.0 for Windows (SPSS Inc., USA).
The relative contributions of three potential sources, mangrove OC, SPOM and seagrass OC, to the soil OC at the Wori mangrove were examined using the IsoSource software (Phillips and Gregg, 2003), which provided the ranges of source proportional contributions to a mixture when the number of sources was too large to permit a unique solution (>number of isotope systems+1).
3 Results
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3.1 Vegetation biomass
The dominant species was R. apiculate at the Wori mangrove and S. alba also co-dominated the landward station (Table 1). The three stations had similar plant densities, ranging from 1 967 stem/hm2 to 2 500 stem/hm2. Higher DBH of R. apiculata was measured at the SW station than other two stations, resulting in higher aboveground and belowground biomasses, and a consequential total biomass than those at the other two stations (p<0.05). There was no significant difference in biomass between the LW and MZ stations.
3.2 Soil carbon stock and carbon source
Soil bulk density, OC concentration and carbon density at the Wori mangrove were 0.31–0.48 g/cm3, 65.97–90.58 mg/g and 25.85–38.05 mg/cm3, respectively (Fig. 1). For the soil cores down to 50 cm collected at the LW and MZ stations, neither sampling station (LW vs. MZ) nor soil depth had a significant effect on the soil bulk density, OC concentration and carbon density at these two stations (Fig. 1 and Table 2). Comparisons of the soil bulk density, OC and OC density of the top 20 cm soil layer among the three sampling stations showed that the values were similar among the three stations or between the two sampling depths (0–10 cm vs. 10–20 cm, Fig. 1 and Table 3).
Mangrove plant had the most 13C-depleted OC in this study with a mean value of (–29.5±0.7)‰, and its OC concentration was (44±2)%. The δ13C of seagrass and SPOM were (–11.1±0.7)‰ and (19.5±0.8)‰, respectively.
The soil δ13C values at the LW and MZ stations showed a spatial variation while the variation was depth-specific (Fig. 2, Table 2). Soil 13C was more depleted in the top 40 cm soil at the LW station than the MZ station, and the soil δ13C in the 40–50 cm soil was similar between the two stations. In the top 20 cm soil, the OC was more enriched in 13C at the SW station (>–28‰) than the other stations, and the δ13C significantly decreased toward landward, with a value <–28.7‰ at the LW station (Fig. 2, Table 3).
δ13C analysis revealed that mangrove OC was the major source of the soil OC (contributing 81% to 95%) at the Wori mangrove, while its contribution slightly decreased from the landward toward the sea (Table 4). The marine source (including SPOM and seagrass) contributed only 0%–19%, and the seagrass had less contributions than SPOM.
3.3 Ecosystem carbon stock
Soil OC stocks were 16.3 kg/m2 and 16.2 kg/m2 in the top 50 cmsoil at the LW and MZ stations (Fig. 3), respectively. Considering that no significant difference in soil OC density was observed with soil depth down to 50 cm at these two stations and the OC stocks in the top 20 cm soil (6.1 kg/m2 for LW and 6.2 kg/m2 for MZ) accounted for ~40% of the total stocks in the top 50 cm soil, we further estimated the soil OC stock in the top 50 cm soil as 13.6 kg/m2 at the SW station from the top 20 cm stock using a conversion factor 2.5 .
Mangrove biomass OC stocks were 60, 60 and 164 Mg/hm2 at the LW, MZ and SW stations, respectively (Fig. 3) and the value was higher at the SW station (p<0.05). The ecosystem OC stock as the sum of mangrove biomass stock and soil stock (in top 50 cm soil) was 22 kg/m2 at the LW and MZ station, while the SW station had a higher stock. The mean ecosystem OC stock, biomass OC stock and soil OC stock were 23.7, 8.3 and 15.4 kg/m2, respectively at the Wori mangrove, and soil OC stock accounted for 65% of the ecosystem OC stock.
4 Discussion
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Previous studies have suggested mangrove wetlands as substantial carbon stocks and the soil OC pool generally represented the majority of ecosystem OC stock (Twilley et al., 1992; Donato et al., 2011; Murdiyarso et al., 2015; Rovai et al., 2018). In the present study, the OC stocks were quantified in the top 50 cm soil and the values ranged from 137 to 164 Mg/hm2 at the Wori mangrove in North Sulawesi, Indonesia. Here we normalized the soil OC stock obtained at the Wori mangrove and those previously reported at other worldwide mangroves at various soil depths (Table 5) to make comparisons, on bias of the previous finding that soil OC density did not differ significantly with depth in mangrove forest (Murdiyarso et al., 2015). Murdiyarso et al. (2015) suggested that the decrease in soil OC concentration with depth was compensated by the increased bulk density (Murdiyarso et al., 2015). The top 1 m soil OC stock at Wori mangrove, equivalent to 274–328 Mg/hm2, fell into the range reported in other mangrove wetlands (Fig. 4). The Wori mangrove also had similar OC stocks in the top 1 m soil to those obtained from other Indonesian mangroves ranging from 270 to 530 Mg/hm2, and had comparable soil OC concentrations to most of the values at these Indonesian mangroves (Murdiyarso et al., 2015). The mean soil OC concentration in present study (79.85 g/kg) was higher than the global median value (20 g/kg) for mangroves (Kristensen et al., 2008), further indicated the Wori mangrove as a substantial soil carbon stock.
The soil carbon stock changed as a function of soil carbon concentration, bulk density and the total depth. By comparing the soil OC stock from various tropical mangroves, Donato et al. (2011) concluded that soil carbon concentration was lower in estuarine sites (with a mean of 7.9 %) than in oceanic (with a mean of 14.6 %) sites, and the mean C densities was also lower in estuarine (0.038 g/cm3) than in oceanic soils (0.061 g/cm3). However, the low OC density of estuarine mangrove soil was compensated by their deeper alluvial soil deposits, resulting in the comparable soil stocks between these two geomorphic settings (Donato et al., 2011). A later review by Breithaupt et al. (2012) also indicated no statistical difference in soil carbon burial rate, which was related to the soil OC sequestration capacity, between the estuarine/riverine and oceanic mangroves. These results suggested that mangroves under these two geomorphic sets are both important in the soil carbon stock and sequestration.
The mangrove soil carbon stock was influenced by the tidal gradient, vegetation biomass and production, species composition and input of allochthonous sources (Gleason and Ewel, 2002; Sherman et al., 2003; Cerón-Bretón et al., 2011). Some estuarine mangrove showed spatial variations in soil OC concentrations and stock, with values increasing from the lower tidal elevation zone toward the land (Chen et al., 2012; Wang et al., 2013). This maybe partially due to the higher biomass and production at the higher-tidal-elevation zone that provide more dead roots and litter into the soil (Wang et al., 2013). Moreover, heavy siltation occurs in the estuarine mangrove resulting in an extensive gradual intertidal slope, and the reduced wave energy and current velocity at the station proximal to the land would facilitate the burial of particular organic matter, and reduce the loss of litter carbon from the mangrove floor. However, there was no significant difference in soil OC concentration and stock among the three sampling stations in this study. This is similar to the finding by Donato et al. (2011) that soil OC density was not variable with the distance from the seaward edge in oceanic mangrove sites. The results further suggested that the spatial variation of soil OC stock was different between the oceanic and estuarine mangroves.
A wide range of mangrove ecosystem OC stocks has been reported worldwide with soil OC stock at various depths combined, from 80.0 Mg/hm2 in Sundarbans in Bangladesh to 1 396.9 Mg/hm2 in Bintuni in Indonesia (Table 5). The ecosystem carbon stocks including the top 1 m soil stock varied from 140. 7 to 874.8 Mg/hm2 and showed higher values in the tropic mangroves than the subtropics (Fig. 4). This was coincided with the previous finding that primary or mature mangrove forests in the tropics in low latitudes had much higher biomass than those in temperate areas on a global scale (Komiyama et al., 2008). The production of mangrove has also been found to exhibit a pronounced geographical trend, with highest litter fall rates measured near the equator and decreased with increasing latitude (Alongi, 2002; Bouillon et al., 2008). Moreover, our results further prove that soil pool was the majority of ecosystem carbon stock (Donato et al., 2011; Alongi et al., 2016) and the soil OC stock (in the top 1 m) accounted for 76% of the ecosystem OC stock at the Wori mangrove. The mean ecosystem OC stock, 391.4 Mg/hm2at the Wori mangrove was lower than other mangroves with similar latitudes, due to the lower biomass OC stock at Wori (Fig. 4). The biomass carbon stock in present study, with an average of 83.4 Mg/hm2 was much less than most of the values reported in other Indonesian mangroves (Fig. 4).
Mangrove derived OC were generally the major source of the carbon accumulated in mangrove soils, while allochthonous organic matter may increase in importance when high rate of input from riverine or tidal sources were presented (Jennerjahn and Ittekkot, 2002). In the present study, the mangrove soil was depleted in 13C and the δ13C was around –28‰. The isotope mixing calculations showed that the rich OC in soil was attributed to the accumulated autochthonous mangrove source. The mangrove contribution (81%–96%) was much higher those reported in other mangrove forests (Gonneea et al., 2004; Muzuka and Shunula, 2006; Ranjan et al., 2011; Tue et al., 2011). For example, Alongi et al. (1998) reported that mangrove carbon represented only 56% of the total OC input to Hinchinbrook Channel while in a lagoon-fringe mangrove the contribution of mangrove OC was found <80% for the soil OC. Although seagrass meadow occurred at the seaward edge of the Wori mangrove, the seagrass derived OC contributed a negligible proportion to the mangrove soil OC in this area, and even if at the seaward station adjacent to seagrass the contribution of seagrass was less than that of SPOM. This was contrarily to previous finding that seagrass could be an important OC input to mangrove soil (Wooller et al., 2003; Walton et al., 2014). Wooller et al. (2003) found that the source of OC in a mangrove soil was primarily allochthonous including seagrass material, and in the Arabian Gulf in-welling of seagrass production balanced the out-welling of mangrove production in the arid mangrove forest (Walton et al., 2014). These findings suggested that the OC flux between mangrove and seagrass could be geographically variable, and the mechanism driving such variation deserved further studies.
Acknowledgements
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The authors are grateful to Asep Rasyidin, Mochtar Djabar and Liang Cuicui for their assistance with field sampling and laboratory analysis.
Funding
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  • The China-Indonesia Ecological Station Establishment and Marine Biodiversity Investigation in North Sulawesi Sea; the Development and Implement Ocean Strategic Planning and Policy supported by Ministry of Natural Resources, PRC; the National Natural Science Foundation of China under contract Nos 41606105 and 41776102.
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Year 2018 volume 37 Issue 12
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doi: 10.1007/s13131-018-1290-5
  • Receive Date：2017-06-15
  • Online Date：2026-04-14
  • Published：2018-12-25
Article Data
Affiliations
History
  • Received：2017-06-15
  • Accepted：2018-03-12
Funding
The China-Indonesia Ecological Station Establishment and Marine Biodiversity Investigation in North Sulawesi Sea; the Development and Implement Ocean Strategic Planning and Policy supported by Ministry of Natural Resources, PRC; the National Natural Science Foundation of China under contract Nos 41606105 and 41776102.
Affiliations
    1 Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
    2 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia
    3 Technical Implementing Unit Marine Life Conservation Biak, Indonesian Institute of Sciences, Biak 98152, Indonesia

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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