Liu et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-020-00387-3(2020) 7:71

Progress in Earth andPlanetary Science

RESEARCH ARTICLE

Open Access

Increase of organic carbon burial response
to mangrove expansion in the Nanliu Riverestuary, South China Sea
Tao Liu1,2, Shengfa Liu3,4* , Bin Wu3, Huipeng Xu1 and Hui Zhang3

Abstract
Due to high productivity, periodic submersion, and rapid sedimentation rate, mangroves are important carbon sinksin tropical-subtropical coastal zones. Mangrove expansion can significantly enhance burial carbon storage in coastal
zones and has been reported in many subtropical regions due to climate change in recent years. To better
understand the response of carbon storage to climate change in subtropical-tropical coastal zones, it is necessary toestimate the change in burial organic carbon (OC) storage in mangroves undergoing expansion. In the Nanliu Riverestuary of South China, the total mangrove area has increased from 72 to 622 ha in recent decades. Based on asedimentology study combined with historical satellite images analysis, the accumulation rate of burial OC in thesemangroves is estimated to be 400–500 g‧m−2‧y−1, of which the part imported to the stratigraphy beneath themangrove deposit layer is approximately 130 g‧m−2‧y−1. Globally, the reported OC accumulation rate is linearlycorrelated to the accretion rate in mangroves. The accumulation rate of mangrove burial OC estimated in this study
is significantly higher than the corresponding value on this fitted curve, indicating that the OC accumulation rates
may be underestimated in such mangroves because the OC imported to the lower root layer has been not beentaken into account. Based on the estimated OC accumulation rate and the time-series data of the mangrove area,
the increase in burial OC storage in the mangroves of the Nanliu River estuary from 1988 to 2018 is estimated atmore than 35 Gg. This study provides an example of estimating soil OC storage increase in expanding mangroves,which can help us better understand the response of coastal carbon pool to climate change.
Keywords: Climate change, Mangrove, Accumulation rate, Organic carbon burial, South China Sea

1 Introduction
Mangrove sediment can sequester a large amount oforganic carbon (OC) due to the high primary productivity,
rapid accretion rate, and water-logged anaerobic soil
environment of mangroves (Mcleod et al., 2011; Alongi,
2014; Jardine and Siikamäki, 2014). Although mangroves
only cover 0.5% of the global coastal area, they account for
10–15% of coastal sediment OC storage (Donato et al.,2011; Ezcurra et al., 2016). The total mangrove area of the* Correspondence: liushengfa@fio.org.cn
3
Key Laboratory of Marine Geology and Metallogeny, First Institute of
Oceanography, Ministry of Natural Resources, Qingdao 266061, China
4
Laboratory for Marine Geology, Qingdao National Laboratory for Marine
Science and Technology, Qingdao 266061, China
Full list of author information is available at the end of the article

world has decreased sharply in the past century mainly
due to human-induced land-use change (Giri et al., 2011).
However, in recent decades, mangroves in many subtropical regions are reported to have expanded due to climatechange (Pérez et al., 2017; Saintilan et al., 2014a; Cavanaugh et al., 2014; Liu et al., 2017).
To estimate the increase in carbon storage by mangroves, the increase in burial OC storage due to mangrove
expansion should be determined. In the Nanliu River estuary of South China, mangroves have replaced most of thesalt marsh and have expanded into bare flat land due to increases in rainfall. This has resulted in a significant increasein the mangrove area from 73 ha in 1988 to 622 ha in
2018. The aim of this study is to determine the burial OC© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
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Liu et al. Progress in Earth and Planetary Science(2020) 7:71

accumulation rate and the increase in burial OC storage
due to the expansion of mangroves in this area. Based ondivisions of the sedimentary facies in two sediment cores,
the amount of burial OC related to the presence ofmangroves was calculated using the depth profile of OC
density. Using the age of mangrove plants determined byhistorical satellite image analysis, the accumulation rate ofburial OC in mangroves was calculated. Furthermore,using the OC accumulation rate and the time series of themangrove area, the increase in burial OC storage from1987 to 2018 was estimated. To estimate the storage ofOC related to mangrove forests, it is necessary to identify the mangrove deposit layer in stratigraphy. By
studying the OC content, sand content, and plant
residual in sediment cores, three kinds of sedimentary
facies can be identified.

2 Study area and methods
This study was conducted in the Nanliu River estuary along
the northern coast of the South China Sea (Fig. 1). The
study area is influenced by a subtropical monsoon climate.
During the past 60 years, the average annual temperature

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was 22 °C and the average annual rainfall was approximately 1600 mm. With an average tidal range of 2.5 m, thediurnal tide dominates in this region. Large mangroves
grow on the upper tidal flat of the river mouths. The vegetation mainly consists of Aegiceras corniculatum, with asmall number of Kandelia candel as well as Sonneratia apetala. The plant height is in the range of 1–4 m. An increasein river discharge during this period is thought to have triggered the rapid expansion of mangroves, a significant expansion of mangroves in Nanliu River estuary during past
decades could be found in Fig. 2.
In 2017, two sediment cores (100 cm in length and 5
cm in diameter) were collected from a mangrove forest
off the mouth of the Nandongjiang River (a distributaryof the Nanliu River). Core C3 was collected in a relatively older mangrove patch (~20–30 years) while coreC7 was collected from a young mangrove patch of approximately 10 years (as inferred using satellite remotesensing images). The sediment cores were sectioned in
2 cm intervals. Then, once the fresh roots were removed,
each subsection was analysed for dry bulk density, totalorganic carbon (TOC), and grain size in a laboratory.

Fig. 1 Study area (a)and the spatial distribution of mangroves off Nanliu River mouth (b), mangroves are marked by the red area, the position of
sediment cores is marked too (c)Liu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 2 The significant expansion of mangroves in Nanliu River estuary during past decades

We utilised a mini ring-knife and a drying oven to determine the dry bulk densities. TOC was measured witha Shimadzu SSM-5000A organic carbon analyser. For
sediment grain size analysis, we used a MasterSizer-3000
laser particle size analyser made by the Malvern Company. Firstly, calcareous clastic and organic matter were
removed using 5% HCl and 10% H2O2 solution, respectively. Secondly, 6% (NaPO3)6 solution was added as adispersing agent while the solution was stirred with aglass rod. Thirdly, the sample was added to the laser
particle size meter for particle size measurement. Finally,
the excess 210Pb radioactivity of the sediment samples
was detected by a α-multichannel spectrometer in theState Key Lab of Lake Sciences of China.

3 Results
3.1 Mangrove deposit layer identification in stratigraphy

In core C3, as the depth increased, deposits of mangrove, salt marsh, and bare flat sediment emerged inturn (Fig. 3). The mangrove deposit (0–22 cm layer) wascharacterised by high OC content (3–4%) and stable low
sand content (approximately 20%). Residual mangrove
litter can also be found in this layer. The salt marsh
deposit (depth range 22–46 cm) was characterised byrelatively high OC content (2–3%) and fluctuating sandcontent (15–40%). The residual of salt marsh plantpetioles can also be found in this layer. The bare flat
sediment deposit constitutes the layer below 46 cm andis characterised by low OC content (1–2%) and highsand content (40–60%). In core C7, collected in young
mangroves which colonised bare flat sediment after
2005, the mangrove deposit layer directly overlays thebare flat deposit. Here, the bare flat deposit is only 10
cm in thickness.

based on historical satellite images (Fig. 4), according towhich we can judge that the mangrove colonising thesite where core C3 was taken (‘C3 site’) in 1992 or 1993.
The mangrove plants at this site were approximately
24 years old in 2017. Given that the thickness of themangrove deposit layer was 22 cm (Fig. 3), the accretion rate in the mangroves of this site is thus around
9 mm/a. Historical satellite images show that the C7
site was located just at the margin of the mangrovein 2005. At the end of 2009, the mangrove patch ofthis site was very clear, indicating the adjacent canopies have been in full touch. This needs more than
3 years in this area. The mangrove colonised there
most likely during 2005–2007. The age of the mangrove plants at the C7 site was no more than 12 years
in 2017. Given the thickness of the mangrove deposit
layer at this site was 12 cm (Fig. 3), the accretion ratein the mangrove is therefore estimated at more than
10 mm/a.
In addition to the analysis based on historical satellite
images, we also calculated the accretion rate using theexcess Pb210 radioactivity in core C3. As shown in Fig. 5,
except for some abnormal data, excess Pb210 radioactivity in the sediment declined exponentially with depth.
Using the CS-CF modal, the accretion rate was calculated at 9.1 mm/a in the mangrove deposit layer and 11
mm/y in the salt marsh deposit layer. The mangrove isthus estimated to be 22 years old. The accretion rate of
the mangrove deposit layer calculated by the Pb210
method is almost the same as that determined using
historical satellite images analysis, indicating the validityof historical satellite images analysis in estimating theage of young mangroves.
3.3 Accumulation rate of burial OC in mangroves

3.2 Age of mangrove plants and accretion rate inmangroves

To estimate the accumulation rate of OC in mangroves,
it is necessary to determine the age of the mangroves. In
this study, we estimated the age of mangrove plants

Based on the division of sedimentary facies, the amountof OC buried in the mangrove deposit layer and the OC
imported to the lower layer can be respectively calculated. At the position of core C7, the burial OC stored in
the mangrove deposit layer was calculated to be 4436 g

Liu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 3 The division of sedimentary facies in tidal flat stratigraphy

per square meter (Fig. 6a, Table 1). In the bare flat
deposit layer below 40 cm, OC density is stable and wasapproximately 0.022 g‧cm−3 on average. In the upper
part of the bare flat deposit layer (12–40 cm), the OC
imported by mangrove roots resulted in an abrupt
increase in OC density. The amount of OC per square
meter sourced from mangrove roots in this layer is thus
determined by subtracting the background OC (5520 g)from the total OC (7074 g) and is approximately 1554 g.
At this site, the total burial OC related to mangroves isthus 5990 g. Given that the mangrove age at this site
was around 12 years at the time of core extraction, thetotal accumulation rate of burial OC related to mangrovesis around 500 g‧m−2‧y−1, in which the accumulation

rate of OC imported to the lower layer is estimatedat 130 g‧m−2‧y−1.
At the position of core C3, the amount of burial
OC per square meter in the mangrove deposit layer iscalculated to be 6498 g. The amount of OC storageby mangrove roots cannot be determined because ofits mixing with the OC from the salt marsh (Fig. 6b).
However, we can estimate the OC imported to thelower layer using the data of core C7. Given that theage of the mangrove at this site is around 24 years,
the OC imported to the lower layer is estimated tobe 3120 g‧m2. Using this data, the total OC related tomangroves and the total OC related to the salt marsh
are determined as 9618 g‧m−2 and 5655 g‧m−2, respectively.

Liu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 4 Position of sediment cores and the spatial distribution of mangrove and salt marsh in satellite images (from landsate and Google earth)Fig. 5 Depth profile of excess Pb210 radioactivity in core C3

Liu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 6 Depth profile of burial OC density in sediment cores C3 and C7

The accumulation rate of burial OC related to mangroves isthus estimated at 400 g‧m−2‧y−1 (Fig. 7).

the mangroves of the Nanliu River estuary over the past
30 years is estimated at approximately 35 Gg.

3.4 Increase in burial OC storage in expanding mangroves

4 Discussion
In the Nanliu River estuary, the accumulation rate ofburial OC in mangroves ranged from 400–500 g‧m−2‧y−1.
The highest value was observed in a young mangrovewith low substrate elevation, where the OC content insediment was higher than in the older mangrove. Thiscan be attributed to the lower decomposition rate of organic debris in the sediment combined with a higher
sediment rate and longer inundation time (Alongi et al.,2005; Nguyen et al., 2004).
The accumulation rate of burial OC in mangroves isgenerally estimated by multiplying the OC content withthe sediment accumulation rate in the mangrove deposit
layer. The OC imported to the stratigraphy beneath theUsing the estimated accumulation rate of burial OC in
the mangrove and the time series of the mangroves of
the Nanliu River estuary from 1988 to 2018, we estimated the variations of OC storage in the Nanliu Riverestuary during this period. As shown in Fig. 8, the increase in burial OC storage in each year was calculated
by multiplying the burial OC accumulation rate with themangrove area for that year. The time series of burial
OC storage increment were then summed to determine
the total increase in burial OC storage during thisperiod. In this study, we used the accumulation rate ofburial OC in core C3 (400 g‧m−2‧y−1) as a conservative
estimate. Using this, the increase in burial OC storage inTable 1 Amount of burial OC ( per square meter)related to mangrove and salt marsh
Position

OC stored in mangrove
deposit layer

OC imported to beneathlayer by mangrove root

Total OC related
to mangrove

Total OC related
to salt marsh

C74436 g1554 g5990 g–

C36498 g

3120 g9618 g5655 gLiu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 7 Accumulation rate of burial OC in mangrove and salt marsh

mangrove deposit layer may be neglected, especiallywhen the sediment core is not long enough to cover thewhole depth range of the mangrove root network. The
results of this study suggest that in a young Aegiceras
corniculatum forest, the accumulation rate of OC
imported to the lower layer is around 130 g‧m−2‧y−1,
which was 26–32% of the total estimated OC accumulation
rate. This evidence suggests that the burial OC accumulation rate in mangroves may be significantly underestimatedif we neglect the OC imported to the lower layer.
According to published data gathered around theworld, the relationships between the OC accumulation
rate and the sediment accretion rate in mangroves canbe well described by a linear law. This linear law is also
valid for the data of this study if we neglect the OC
imported to the stratigraphy beneath the mangrove deposit layer (Fig. 9). However, the total OC accumulation
rate estimated in this study is significantly higher than
this fitted curve, indicating that the OC accumulation

rate is likely to be undervalued in many mangroves aroundthe world. On the other hand, in the regions where
mangroves have replaced salt marsh, the lower salt marsh
deposit layer can be mistaken for mangrove deposit. Given
that the OC accumulation rate in the salt marsh is usually
lower than that in the mangrove forest, the mangrove burial
OC accumulation rate may be undervalued.
Due to climate change, mangroves have been expanding into salt marsh areas in many regions in recent years(Comeaux et al., 2012; Saintilan et al., 2014b; Liu et al.,2017). The increase of OC burial in such mangroves is
considerable. Estimating the increase in burial carbon
storage in mangroves undergoing expansion is an important scientific task that will allow for a better understanding of changes in coastal carbon storage. Traditionally,changes in burial OC storage in mangroves during acertain period may be estimated using the burial OC
accumulation rate, mangrove patch area, and time span.
This method may be valid for stable mangroves with a

Fig. 8 a Time series of mangrove area from 1987 to 2018 in Nanliu River estuary; b increment of burial OC in Nanliu River estuary

Liu et al. Progress in Earth and Planetary Science(2020) 7:71

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Fig. 9 The relation between accretion rate and OC accumulation rate in mangroves around the world (the data used here are revised fromMacKenzie et al., 2016; Smoak et al., 2013; Pérez et al., 2017; Yang et al., 2014)

fixed area, but may not be valid for expanding mangroves.
A new method must therefore be developed to solve thisproblem. In this study, we show an effective method for
estimating the increase in the burial OC storage of mangroves undergoing expansion. Besides the accumulation
rate of burial OC, this method requires the burial OC accumulation rate and the time series of the mangrove area.
The increment of burial OC storage in the mangrove foreach year is calculated by multiplying the OC accumulation rate with the mangrove area of that year. Then, thetotal increase in burial OC during this period is estimatedby summing the time series of burial OC increment. Since
plenty of satellite images have been taken during past
decades, we can accurately establish the time series ofmangrove area in a certain region. The regional increaseof OC burial in mangroves thus can be obtained easily by
this method. With global warming, mangrove expansion
may take place in the regions of higher latitude. According
to the process and rate of mangrove expanding in a similar environment, the future change of OC burial in coastal
wetlands of a certain area also can be predicted by thismethod. This can help us in evaluating the response ofcoastal carbon pool to climate change.

OC accumulation rates of mangroves in the Nanliu Riverestuary were estimated. The results show that the OC
accumulation rate in these mangroves is approximately
400–500 g‧m−2‧y−1, of which the OC imported to thelower layer of the mangrove roots is approximately
130 g‧m−2‧y−1.
(2) Globally, reported burial OC accumulation rates inmangroves are well linearly correlated to the accretion
rate. In this study, however, the total OC accumulation
rates are significantly higher than the corresponding
value on the fitted curve, indicating that the burial OC
accumulation rates may be undervalued in these mangroves because the OC imported to the lower layer bymangrove roots has been neglected.
(3) Using an integrated method, we utilised the burial
OC accumulation rate and the time series of the mangrove area from 1988 to 2018 to estimate the increase inburial OC storage in mangroves. By our estimate, burial
OC storage by mangroves amounts to more than 35 Gg
over this 30 year period.

5 Conclusions(1) Based on the division of sedimentary facies from two
sediment cores and estimates of mangrove age determined by historical satellite image analysis, the burial

Authors’ contributions
TL participated in the data analysis and research idea design and completed
the main work of the paper. SFL conceived of the study and participated inits design and coordination. BW participated in the data analysis and drafted
the manuscript. HPX participated in the sample analysis and drafted the

Acknowledgements
We would like to thank Mr. Lianghao Pan, Mr. Yancheng Tao, and Mr. Wenai
Liu for sediment samples collecting.

Liu et al. Progress in Earth and Planetary Science(2020) 7:71

manuscript. HZ participated in the sample analysis and drafted themanuscript. All authors read and approved the final manuscript.
Funding
This work was supported by the National Nature Science Foundation ofChina-Shandong Province Joint Fund for Marine Science Research Centers(U1606401), National Programme on Global Change and Air-Sea Interaction(GASI-GEOGE-03), and Taishan Scholar Program of Shandong.
Availability of data and materials
The dataset supporting the conclusions of this article can be found in the
supplementary files.

Page 9 of 9Saintilan N, Wilson NC, Rogers K, Rajkaran A, Krauss KW (2014a) Mangrove
expansion and salt marsh decline at mangrove poleward limits. Global
Change Biol 20:147–157
Saintilan N, Wilson NC, Rogers K, Rajkaran A, Krauss KW (2014b) Mangrove
expansion and salt marsh decline at mangrove poleward limits. Global
Change Biol 20:147–157
Smoak JM, Breithaupt JL, Smith TJ, Sanders CJ (2013) Sediment accretion andorganic carbon burial relative to sea-level rise and storm events in two
mangrove forests in everglades national park. Catena 104(2):58–66
Yang J, Gao J, Liu B, Zhang W (2014) Sediment deposits and organic carbon
sequestration along mangrove coasts of the Leizhou Peninsula, southern
China. Estuarine, Coastal and Shelf Science 136:3–10

Publisher’s Note
Competing interests
The authors declare that they have no competing interests.
Author details
1
School of Marine Sciences, Guangxi University, Nanning 530004, China. 2Key
Laboratory of Environment Change and Resources Use in Beibu Gulf, Ministryof Education, Guangxi Teachers Education University, Nanning 530004, China.
3
Key Laboratory of Marine Geology and Metallogeny, First Institute of
Oceanography, Ministry of Natural Resources, Qingdao 266061, China.
4Laboratory for Marine Geology, Qingdao National Laboratory for Marine
Science and Technology, Qingdao 266061, China.
Received: 22 June 2020 Accepted: 3 November 2020

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