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Science of the Total Environment 793 (2021) 148568

Contents lists available at ScienceDirect

Science of the Total Environment

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

The first national scale evaluation of organic carbon stocks and


sequestration rates of coastal sediments along the West Sea, South Sea,
and East Sea of South Korea
Jongmin Lee a, Beomgi Kim a, Junsung Noh a, Changkeun Lee a, Inha Kwon a, Bong-Oh Kwon b, Jongseong Ryu c,
Jinsoon Park d, Seongjin Hong e, Sukhui Lee f, Seong-Gil Kim f, Sujin Son g, Hoon Joo Yoon g, Jongseo Yim h,
Jungho Nam h, Kyungsik Choi a, Jong Seong Khim a,⁎
a
School of Earth and Environmental Sciences & Research Institute of Oceanography, Seoul National University, Seoul 08826, Republic of Korea
b
Department of Marine Biotechnology, Kunsan National University, Kunsan 54150, Republic of Korea
c
Department of Marine Biotechnology, Anyang University, Ganghwa-gun, Incheon 23038, Republic of Korea
d
Department of Ocean Science, Korea Maritime and Ocean University, Busan 49112, Republic of Korea
e
Department of Ocean Environmental Sciences, Chungnam National University, Daejeon 34134, Republic of Korea
f
Korea Marine Environment Management Corporation, Seoul 05718, Republic of Korea
g
Department of GeoAI, Sundosoft Ltd., Seoul 08503, Republic of Korea
h
Marine Policy Research Division, Korea Maritime Institute, Busan 49111, Republic of Korea

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• First estimated organic carbon stocks


and sequestration rate in the Korean
tidal flats
• Evidenced terrestrial impacts on sedi-
mentary organic carbon for some tidal
flats of Korea
• Confirmed mud content and halophytes
as key factors affecting coastal sediment
organic carbon.
• Identified the area and sediment tex-
tural types of tidal flats using remote
sensing technique.
• Reported organic C stocks (13 Tg C) and
sequestration rate (71 Gg C yr−1) in
Korean tidal flats

a r t i c l e i n f o a b s t r a c t

Article history: Blue carbon science requires the estimates of organic carbon stock and sequestration rate; however, holistic data
Received 25 March 2021 analysis remains limited in South Korea. The present study reports current organic carbon stocks and sequestra-
Received in revised form 24 May 2021 tion rates in the coastal areas of West Sea, South Sea, and East Sea of South Korea, encompassing entire intertidal
Accepted 16 June 2021
areas using long-term field survey combined with remote sensing technology. Twenty-one intertidal flats were
Available online 23 June 2021
targeted across seven provinces (Gyeonggi, Chungnam, Jeonbuk, Jeonnam, Gyeongnam, Gyeongbuk, Gangwon).
Editor: Paola Verlicchi Out of the evaluated environmental parameters, mud content represented a significant factor controlling
sedimentary organic carbon stocks across target areas, and was significantly positively correlated to the total
organic carbon (p < 0.05). Organic carbon stocks measured in salt marshes (i.e., upper intertidal zone) reflected
Keywords: the high carbon fixation capacity of halophytes through primary production. Sediment textural type was
Total organic carbon

⁎ Corresponding author at: School of Earth and Environmental Sciences & Research Institute of Oceanography, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826,
Republic of Korea.
E-mail address: jskocean@snu.ac.kr (J.S. Khim).

https://doi.org/10.1016/j.scitotenv.2021.148568
0048-9697/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

Sequestration rates classified using analysis of remotely sensed imagery, and was closely correlated to field-based classification data
Blue carbon (p < 0.05). Using field and remote sensing results, we estimated total organic carbon stocks (13,142,149 Mg
Remote sensing classification C) and sequestration rates (71,383 Mg C yr−1) in the tidal flats of South Korea. This study presents the first report
Net-zero carbon
on blue carbon potential in the Korean tidal flats, providing baseline information on the carbon dynamics of
Korean tidal flats
intertidal sediments in this region and, potentially, elsewhere.
© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction overcome the limitation of field surveys and laboratory analyses, partic-
ularly for large scale estimations.
Recently, researchers have highlighted the role of coastal ecosys- South Korea is located in the eastern part of the East Asia between
tems under global warming, with respect to coastal protection and China and Japan. The Korean Peninsula has three main coastlines
buffering and for regulating “Blue Carbon” services (Mcleod et al., (east-, west-, and south-facing) abutting the East Sea, West Sea, and
2011). Coastal sediment represents a dominant reservoir of seques- South Sea, respectively. The region extending from western coast to
tered organic carbon in marine environments, and has an important the southern coast of Korea is connected geographically to the eastern
ecological role in global biogeochemical carbon cycling (Hedges part of the Yellow Sea. This region has a shallow shelf (<200 m of
et al., 1997; Kubo and Kanda, 2017). Salt marshes and other coastal water depth) and an archipelago with strong macrotidal conditions
ecosystems (mangroves and seagrasses) are representative blue car- (4–9 m) (NGII, 2016). As a result, there are extensive tidal flats
bon habitats, due to their serving as highly efficient CO2 sinks (~2,500 km2), along the western and southern coasts of Korea (Fig. 1).
(Chmura et al., 2003; Mcleod et al., 2011; Kelleway et al., 2016). Such environmental conditions potentially favor the burial and/or se-
For example, coastal vegetated ecosystems, such as salt marshes, questration of organic matter; however, there have been no studies on
contribute to almost 50% of carbon sequestration in marine sedi- this phenomenon at a national scale in Korea.
ments, despite occupying only 0.2% of the ocean surface (Chmura The present study investigated how various parameters drive spa-
et al., 2003; Mcleod et al., 2011; Duarte et al., 2013; Kelleway et al., tiotemporal variation in the organic carbon stock of coastal sediments
2016). Recently, several studies have demonstrated that global along the West Sea, South Sea, and East Sea of Korea. The targeted end-
blue carbon habitats store up to 1.02 Pg CO2 yr−1, which is equiva- points included total organic carbon, organic carbon stock, organic car-
lent to 3–19% total carbon emission by deforestation, globally bon sequestration rate, mud content in the tidal flat areas of Korea. The
(Pendleton et al., 2012; Macreadie et al., 2019). This phenomenon specific objectives were to: (1) investigate regional and temporal varia-
exists because salt marshes are highly productive ecosystems that tions of organic carbon stock per unit area; (2) elucidate environmental
convert plant biomass carbon from CO2 through primary production, factors affecting sedimentary organic carbon; (3) evaluate the relation-
and deposit biomass carbon in sediments over long-periods (Duarte ship between biogeochemical properties (e.g., sediment grain size and
et al., 2013; Spivak et al., 2019). vegetation) and sedimentary organic carbon; (4) determine the accu-
Sedimentary organic carbon in coastal areas originates from both racy of remote sensing classification for sediment textual types com-
terrestrial and marine sources, with quantities varying depending on pared to experimental (field-based) classification; and (5) identify
the source (Graham et al., 2001; Lamb et al., 2006; Kubo and Kanda, sedimentary organic carbon stocks and sequestration rates in South
2017). Anthropogenic inputs (e.g., industrial, aquacultural, and munici- Korea. Overall, the present study aimed to present a national-scale eval-
pal sewages) from terrestrial areas also contribute to the burial of or- uation of organic carbon stocks and sequestration rates in the tidal flats
ganic carbon in coastal sediments (Rumolo et al., 2011; Pradhan et al., of Korea.
2014). While this phenomenon is widely reported, organic carbon dy-
namics from rivers to the coastal ecosystem remain subject to debate 2. Materials and methods
(Krishna et al., 2013).
Sediment characteristics, such as mud content (silt + clay), repre- 2.1. Study area
sent typical environmental factors that influence the distribution of or-
ganic carbon in the marine ecosystem (Burdige, 2007; Serrano et al., Core sediment samples were collected in 2018 and 2019 from 21
2016). For instance, mud-dominated sediment is mainly composed of regions across provinces (Gyeonggi, Chungnam, Jeonbuk, Jeonnam,
silt and clay, which traps more organic particles compared to sand- Gyeongnam, and Gyeongbuk) of South Korea (Table S1). To identify
dominated sediment, due to the presence of a larger surface area with the quantity and geographic distribution of carbon in tidal flats, 21 re-
higher adsorption capacity (Keil and Hedges, 1993; Burdige, 2007). gions were selected to represent tidal flats along the west, south, and
Thus, the existence of a significant relationship between mud and or- east coasts (Fig. 1). Gyeonggi tidal flats cover ~876 km2 (Ganghwa,
ganic contents means that mud content could be used as a reliable Youngjong, Siheung, Daebu, and Hwaseong), and are located near the
proxy of organic carbon, facilitating the low-cost assessment of blue car- Han River, which is the largest river in South Korea. The Han River estu-
bon stock (Serrano et al., 2016). ary is located on the border between South Korea and North Korea. It
For example, an equation showing the relationship between discharges about 19–25 × 109 m3 yr−1, and flows through the center
organic carbon in bare sediment and mud content was proposed of Seoul.
(R2 = 0.78, p < 0.001): Organic carbon content (%) = 0.06 × Mud Chungnam tidal flats cover ~357 km2 (Garolim Bay, Geungheung,
content (%) − 0.03 (Serrano et al., 2016). Therefore, the strong associa- Ocheon, and Biin), and are located on the western part of the Korean
tion of sediment characteristics with organic carbon should be explored Peninsula. Jeonbuk tidal flats (Seonyudo and Gomso Bay) encompass
to examine carbon geochemical processes. 118 km2, and are located on southwestern part of Korea. Jeonnam
Remote sensing technologies and geographical information systems tidal flats (Hampyeong, Sinan, Aphaedo, Gangjin Bay, Deukryang Bay,
are being increasingly used to obtain reliable estimates of sedimentary Suncheon Bay, and Yeoza Bay) encompass 41.7% (~1,044 km2) of the
organic carbon stock and sequestration rates (Mohamed et al., 2019). remaining tidal flats in Korea (Choi, 2014a). Finally, Gyeongnam tidal
In particular, remote sensing technologies provide useful information flats (Jinhae Bay and Nakdong River estuary) are relatively small in
to estimate organic carbon stock from tidal flat delineation data (Yim size (~92 km2), and are located on the southeastern part of the Korean
et al., 2018). Indeed, the remote sensing technology could be used to Peninsula.

2
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

(a) Organic C stocks Organic C stocks


(Mg C ha-1) Region 126°E 128°E (Mg C ha-1)
150 100 50 0 30
Incheon N 0 50 100 150

1: Ganghwa 1 Gangwon
2
Gyeonggi
2: Youngjong 4 3
5
3: Siheung 37°N
6

4: Daebu 7 South Korea


21 21: Uljin
Chungnam
8
5: Hwaseong Gyeongbuk
9
6: Garolim Bay
10
Ulsan
7: Geungheung Jeonbuk
11 Busan
8: Ocheon Gyeongnam
9: Biin 12 Jeonnam 19 20
35°N
17
10: Seonyudo 13
14
16 18
15 South Sea
11: Gomso Bay

12: Hampyeong 50 km

ay
13: Sinan

r
ay

ive
gB
ay

West East

nB

y
y

ry g R
Ba
nB

Ba
an

eo

tua on
Sea Sea
kry

ae
gji

za
ch
14: Aphaedo

es akd
an

eu

inh
eo
un
:G

:D

:N
:Y

:J
:S

20
15

16

18

19
17

12 8 4 0 0 0 0 4 8 12
Tidal amplitude Tidal amplitude
(m) 50 4 (m)
100 South 8
Sea
150 12
(b) 1: Ganghwa 6: Garolim Bay 13: Sinan 17: Suncheon Bay 20: Nakdong River estuary
150
Organic C stocks
(Mg C ha-1)

100

50
N.A
0
2017 2018 2019 2020 2017 2018 2019 2020 2017 2018 2019 2020 2017 2018 2019 2020 2017 2018 2019 2020

Year

Fig. 1. Map showing the sampling sites along the west, south, and east coasts of South Korea. (a) Spatial distribution of organic carbon stocks in the core sediments of 21 regions of South
Korea. Core sediments were collected from Ganghwa (n = 44), Youngjong (n = 4), Siheung (n = 8), Daebu (n = 8), Hwaseong (n = 8), Garolim Bay (n = 36), Geungheung (n = 8),
Ocheon (n = 8), Biin (n = 10), Seonyudo (n = 8), Gomso Bay (n = 4), Hampyeong (n = 10), Sinan (n = 25), Aphaedo (n = 5), Gangjin Bay (n = 12), Deukyang Bay (n = 6), Suncheon
Bay (n = 32), Yeoza Bay (n = 12), Jinhae Bay (n = 10), Nakdong River estuary (n = 33), and Uljin (n = 12). Yellow, green, and navy shading denotes sedimentary organic carbon stocks
along the west, south, and east coasts, respectively. Mean values of organic carbon stocks for west, south, and east coasts represent yellow, green, and navy lines. Blue lines denote the tidal
amplitude in the West, South, and East Sea. (b) Temporal distribution (2017–2020) of organic stock in five regions (Ganghwa, Garolim Bay, Sinan, Suncheon Bay, and Nakdong River
estuary). Grey lines denote mean values of organic carbon stocks over four years.

2.2. Tidal flat delineation using remote sensing by an intersection algorithm, which is a spatial processing algorithm
generated by overlaying vector layers. This algorithm divides the
The tidal flats along the West, South, and East Sea of South Korea intersected area by calculating the cross points between the
were delineated with intertidal polygon data maps using the QGIS pro- input layer and intersection layer. Overall, tidal flat areas in South
gram (https://www.qgis.org/en/site/). QGIS is a Geographic Informa- Korea were calculated by summing the intersected area of 11,905 grid
tion System (GIS) analysis tool that provides spatial analysis of zones.
geographic information, such as vector and raster images, based on a To delineate tidal flats along the west and south coast, we used
Graphic User Interface (GUI). The study area consisted of 11,905 grid intertidal polygon data maps provided by the Ministry of Oceans and
zones (grid size: 0.9 × 0.9 km2) of an intertidal cover map. The tidal Fisheries (MOF) (Data of 2018). The MOF provides intertidal polygon
flat area delineated in each grid zone was calculated by an intersection data maps and statistical databases (Source: https://kosis.kr/eng/) on
algorithm, which is a spatial processing algorithm generated by overlay- tidal flats once every five years through a national investigation. How-
ing vector layers. The procedure is presented in Fig. S1. First, the ever, intertidal polygon data were not available for the east coast, be-
intertidal polygon and grid zones were overlaid using QGIS. Second, cause of limited data. Thus, we extracted the East Sea intertidal
the intertidal polygons in each grid zone were divided by intersection polygon data maps using Electronic Navigational Chart (ENC) provided
algorithms based on the cross points. Finally, the intersected area by Korea Hydrographic and Oceanographic Agency (KHOA). The proce-
of each grid zone was delineated, and entered on the database following dure involved, first, extracting map data at low-tide and high-tide along
grid IDs. The tidal flat area delineated in each grid zone was calculated the east coasts using ENC. Second, closed curve data were constructed

3
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

by modifying topological errors in ENC data. Finally, we transformed The relationship between excess 210Pb in sediment and age was
closed curve data to intertidal polygon data maps to delineate the east expressed with the following equation (Eq. (2)):
coast.
The similarity of ENC data to MOF data is debatable, due to possible 1 C0
t¼ ln ð2Þ
errors in the analysis process. Thus, the similarity of tidal flat delineation λ Ci
results for the West and South Sea based on ENC data was evaluated in
where t is layer age (yr); C0 is the cumulative activity of all excess 210Pb
the present study. The delineation results using ENC were quantitatively
from the water-sediment interface to the background; Ci is the cumula-
compared with the official MOF data. Specifically, we calculated Mean
tive inventory of 210Pb at depth i (cm); and λ is the radioactive decay
Bias Error (MBE) and Root Mean Square Error (RMSE) between the
constant of 210Pbex (0.03114 yr−1). Both C0 and Ci were be obtained
two datasets for 2,252 grid zones selected from tidal flats along the
by integrating excess 210Pb activity at corresponding intervals in core
west and south coasts (Table S2).
sediments. The sedimentation rate was estimated using the following
equation (Appleby, 2001) (Eq. (3)):
2.3. Validation of sediment textural types using remote sensing
d
The textural type of sediment in the tidal flats of each grid zone was r¼ ð3Þ
t
classified as sand, mixed, and mud based on the judgment of morphol-
ogy, sedimentology, and stratigraphy by an expert marine geologist for where r is the sedimentation rate (cm yr−1); d is the depth of the core
South Korea (coauthor: Choi, K.; for details, see in Choi, 2014b). We ver- sediment (cm); and t is layer age (yr). The sedimentation rate of core
ified this approach by comparing the remote sensing derived data with sediments at the sampling sites is shown in Fig. S2.
experimental classification data (over 2,500 samples were analyzed for
mud contents, covering the 74 unit grid area of 0.9 × 0.9 km2) obtained 2.5. Calculation of organic carbon stock
from the in situ, with the two being statistically significant (p < 0.01;
Table S1). To estimate organic carbon stock per unit area in core sediments, we
followed the standard method of Howard et al. (2014) (Eqs. (4)–(7)).
2.4. Sampling and laboratory analyses
 Mass of dry sediment ðgÞ
Bulk density g cm−3 ¼ ð4Þ
Original volume sampled ðcm3 Þ
To sample core sediments, we used both a cylindrical multisampler
core (diameter = 5 cm) and a semi-cylindrical gouge (diameter = 
Amount carbon in core section gC cm−2
3 cm) depending on whether the substrate was slack (low cohesion) −3

or compact (high cohesion), respectively (Table S3). Core sediments ¼ Bulk density g cm  Organic carbon content ðgCg1 Þ
 Sediment thichness interval ðcmÞ ð5Þ
(60–100 cm; subsamples at 5 cm intervals) from 21 regions along
the western, southern, and eastern coasts of South Korea were sampled
in salt marshes and bare tidal flats from 2018 to 2019, respectively The bulk density data of core sediments in the study areas are shown
(Table S1). To monitor the annual variation in organic carbon in Table S5.
stocks, five regions (Ganghwa, Garolim Bay, Sinan, Suncheon Bay, and  
Summed core carbon gC cm−2 ¼ Amount carbon in core section A gC cm−2
Nakdong River estuary) were selected as representing typical tidal −2

þAmount carbon in core section B gC cm
flats along the west and south coasts of South Korea. In addition, core 
þAmount carbon in core section C gC cm−2
sediments in five target regions were sampled over four years (2017 
þ ⋯ All the samples from a single core gC cm−2
to 2020; Table S4).
To analyze general sediment parameters, samples were stored in air- ð6Þ
tight plastic bags to prevent evaporation, and were subsequently trans-
ferred to the laboratory. Mud content was measured by rapid partial Summed core carbon was calculated using Eq. (6). We also normal-
analysis through wet-sieving (Buchanan, 1984). The sediment textural ized the data for which core depth was <100 cm (Fig. S3). Under the
type was classified by mud (silt + clay) content; 1) sand (sand + normalization method, we assumed that organic carbon contents at
slightly muddy sand, 0–25% mud content), 2) mixed (muddy sand + depths >60 cm were equal to that at 60 cm.
sandy mud, 25–75%), and 3) mud (slightly sandy mud + mud,  
−1
75–100%) (Flemming, 2000). Sediment samples for analyzing total or- Organic carbon stock per unit area Mg C ha

ganic carbon were freeze-dried, homogenized, and powdered using ¼ Summed core carbon gC cm−2  0:01 ð7Þ
agate mortar. To determine TOC, the sediment was decalcified with
10% HCl, washed twice with deionized water, and freeze-dried. TOC where 0.01 is the conversion factor (1 Mg = 1,000,000 g, 1 ha =
was measured using an Elemental Analyzer-Isotope Ratio Mass 100,000,000 cm2) to express unit (Mg C ha−1), that commonly used
Spectrometer (EA-IRMS) (Elementar, Gmbh, Hanau, Germany). The in organic carbon stock assessment.
age of core sediments was calculated using a constant rate of supply To determine the total amount of organic carbon stock (Mg C) in the
(CRS) model for the vertical profiles of excess 210Pb activity (Appleby ecosystem, we multiplied the organic carbon stock per unit area (Mg C
and Oldfieldz, 1983). Excess 210Pb activity was calculated from the ha−1) for each core obtained in Eq. (7) by the tidal flat area (km2)
differences between the activity of supported and unsupported 210Pb. (Eq. (8)).
Supported and unsupported 210Pb activity was measured using
Organic carbon stock ðMg CÞ  
gamma spectroscopy attached to a low background HPGe detector of
−1
the Korea Basic Science Institute (KBSI). All 210Pb dating models used ¼ Organic carbon stock per unit area Mg C ha
excess 210Pb (Krishnaswamy et al., 1971; Sanchez-Cabeza and Ruiz-   100 ha
2
 Tidal flat area km  2
ð8Þ
Fernández, 2012), in which (Eq. (1)): 1 km

210 As part of the analysis, we obtained organic carbon stocks in


Unsupported Pb ¼ 210 Pb
the coastal zones of Ganghwa, Youngjong, Siheung, Daebu, Hwaseong,
Supported
210
Pb ¼ 226 Ra ð1Þ Garolim Bay, Geunheung, Ocheon, Biin, Seonyu, Gomso Bay,
Excess210 Pb ¼ 210 Pb–226 Ra Hampyeong, Sinan, Aphaedo, Gangjin Bay, Deukryang Bay, Suncheon

4
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

Bay, Yeoza Bay, Jinhae Bay, Nakdong River estuary, and Uljin. In this carbon stock (58.1 ± 3.3 Mg C ha−1) compared to those of the west
study, a total of 303 sediment core samples were collected from salt coast (50.3 ± 2.2 Mg C ha−1). Because most of the tidal flats along the
marshes and bare tidal flats in Korea. South Sea are semi-enclosed embayments compared to those of the
West Sea (Koh and Khim, 2014), larger quantities of organic carbon
2.6. Calculation of organic carbon sequestration rate likely accumulate from terrestrial sources (e.g., freshwater algae, plants,
and human activities) (Wang et al., 2018).
The organic carbon sequestration rate was estimated using the fol- In general, the concentration of sedimentary organic carbon showed
lowing equation (Xiaonan et al., 2008; EI-Hussieny and Ismail, 2015) local fluctuations in relation to potential anthropogenic- and natural
(Eq. (9)). sources (Lee et al., 2019). Sources tend to be a mixture of different con-
 tributions of both marine and terrestrial origin, indicating the impor-
Organic carbon sequestration rate per unit area g C cm−2 yr−1 tance of local environments (Graham et al., 2001; Lamb et al., 2006).
 
¼ Bulk density g cm−3  Organic carbon content gC g−1 In the present study, Gyeonggi and Gyeongnam provinces had the

 Sedimentation rate cm yr−1 ð9Þ highest organic carbon stocks of the west and south coasts, respectively
(Fig. 1a). Both provinces are strongly influenced by terrestrial inputs
where bulk density (g cm−3) and organic carbon (g C g−1) are average through freshwater discharge (Choi et al., 2011; Koh and Khim, 2014;
values in the sediment core profile. We then converted Eq. (9) to com- Lee et al., 2018; Lee et al., 2019). Furthermore, riverine inputs of anthro-
monly used unit (Mg C ha−1 yr−1), by implementing a 0.01 conversion pogenic organic matter (such as municipal sewage and discharge) pos-
factor (1 Mg = 1,000,000 g, 1 ha = 100,000,000 cm2) (Eq. (10)). To sibly contribute to the burial of organic carbon in sediments (Bae et al.,
estimate overall organic carbon sequestration rate (Mg C yr−1), we mul- 2017; Lee et al., 2019). For example, high organic carbon stocks in Jinhae
tiplied the organic carbon sequestration rate per unit area (Mg C ha−1 Bay reflect exposure to point-sources of coastal pollutions from indus-
yr−1) for each core (Eq. (10)) by the tidal flat area (km2) (Eq. (11)). try, aquaculture, and municipal sewage discharge since the 1970s
  (Lim et al., 2006; Seo et al., 2014). Overall, terrestrial input considerably
−1
Organic carbon sequestration rate per unit area Mg C ha yr−1 influenced the dynamics of sedimentary organic matter in this province,

¼ Organic carbon sequestration rate per unit area g C cm−2 yr−1 with a strong direct effect from riverine discharge.
 0:01 Furthermore, we investigated temporal variation in the organic
ð10Þ carbon stocks of core sediments from the five target regions (Ganghwa,
 Garolim Bay, Sinan, Suncheon Bay, and Nakdong River estuary) be-
Organic carbon sequestration rate Mg C yr−1   tween 2017 and 2020 (Fig. 1b; Table S4). Temporal variability of organic
−1
¼ Organic carbon sequestration rate per unit area Mg C ha yr−1 carbon stock was generally stable across the five regions over the four-
  100 ha year period. There was no significant difference in the organic carbon
2
 Tidal flat area km  2 stocks of core sediments over the monitoring period in the target re-
1 km
ð11Þ gions. Such stable storage of organic carbon (viz., refractory carbon)
could be generated through a decrease in microbial activity. This
2.7. Statistical analyses phenomenon occurs in the anaerobic conditions of core sediments,
resulting in its contribution to the “Blue Carbon” of tidal flats
SPSS 23.0 (SPSS Inc., Chicago, IL) was used to perform the statistical (Macreadie et al., 2019).
analyses. Organic carbon stocks of core sediments were analyzed to test
for differences between the four survey years (2017, 2018, 2019, and 3.2. Environmental factors affecting the complex dynamics of sedimentary
2020) across five regions (Ganghwa, Garolim Bay, Sinan, Suncheon organic carbon stocks
Bay, and Nakdong River estuary) using one-way analysis of variance
(ANOVA) with Scheffe's post-hoc test. Before the analysis, homogeneity Organic carbon stocks of intertidal sediments along the west, south,
of variance was determined between groups with Levene's homogene- and east coast significantly different with respect to their environmen-
ity test, meeting the assumption of homogeneity of variance (p < 0.05). tal conditions, including geography, salinity, land-use type, vegetation,
To estimate variation in geography, morphology, salinity, land-use, and and mud content (Fig. 2). Although there was no statistically significant
vegetation, we performed t-test. Pearson correlation analysis was used difference in organic carbon stocks with morphology, embayments had
to test for significant relationships with: 1) organic carbon stocks and relatively higher values compared to open coasts. Higher organic carbon
human population, 2) organic carbon stocks and tidal amplitude, 3) or- stocks of brackish water stations seemed to reflect the large quantities
ganic carbon stocks and mud content, 4) organic carbon content and of anthropogenic inputs from industrial and/or municipal sources. In
mud content, and 5) remote sensing classification and mud content. addition, the organic carbon stock of salt marsh significantly differed
to that of bare tidal flat, indicating organic carbon residues originated
3. Results and discussion from halophytes. Human population density, linked to nutrient inputs
from industrial and/or municipal sources (e.g., sewage) (Caccia and
3.1. Spatiotemporal distribution of organic carbon stocks per unit area Boyer, 2007), showed no statistical correlation with organic carbon
stocks (Fig. 2f). For example, low organic carbon stocks of the Nakdong
The data on sedimentary organic carbon stock per unit in the 21 River estuary, which are sand-dominant intertidal flats with the highest
coastal regions generally indicated varied spatial and temporal distribu- population, did not reflect the elevated nutrient loading. Thus, the large
tions (Fig. 1). The topographical characteristics (e.g., coastline, tidal flat quantity of anthropogenic inputs did not seem to contribute as sources
area, and salt marsh area) of the stations in the tidal flats of the West of organic carbon, particularly in the sand-dominated bottoms (Liu
Sea, South Sea, and East Sea of South Korea differed (Table S6). By prov- et al., 2016; Lee et al., 2019).
ince, Gyeonggi (including Incheon) had the greatest organic carbon Interestingly, organic carbon stocks were significantly related to
stock per unit area (81.0 ± 3.3 Mg C ha−1), followed by Southern tidal amplitude in certain regions (Figs. 2g; S4). For example, the
Jeonnam (77.0 ± 3.2 Mg C ha−1), Gyeongnam (including Busan) organic carbon stocks in West Sea and open coasts were positively cor-
(68.3 ± 3.4 Mg C ha−1), Chungnam (35.6 ± 1.9 Mg C ha−1), Western related with tidal amplitude (r = 0.67, p < 0.01 and r = 0.53, p < 0.01,
Jeonnam (33.6 ± 2.2 Mg C ha−1), Jeonbuk (21.3 ± 4.4 Mg C ha−1), respectively), but there were no significant relationships for the
and Gyeongbuk (18.1 ± 1.2 Mg C ha−1) (Fig. 1a). Furthermore, the samples collected in the South Sea and embayment regions. This
tidal flats along the south coast had slightly higher sedimentary organic result suggested that tidal energy under varied topographical and

5
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

(a) Geography (b) Morphology (c) Salinity (d) Land-use (e) Vegetation
150
*p < 0.05 Not significant **p < 0.01 *p < 0.05 **p < 0.01
Organic C stocks
(Mg C ha-1) 100

50

0
West Sea South Sea East Sea Open coast Embayment Brackish Saline Agriculture/ Industrial/ Bare tidal flat Salt marsh
Beach Municipal
(n = 186) (n = 105) (n = 12) (n = 173) (n = 130) (n = 101) (n = 202) (n = 248) (n = 55) (n = 171) (n = 132)

(f) Human population (g) Tidal amplitude (h) Sediment type


150
West Sea Sand Mixed Mud
Organic C stocks
(Mg C ha-1)

100

r = 0.67, p < 0.01 r = 0.60, p < 0.01


50

0
0 20 40 60 80 100 0 2 4 6 8 10 0 20 40 60 80 100
Population (1 x 10,000) Tidal amplitude (m) Mud content (%)

Fig. 2. Distribution of organic carbon stocks in core sediments with respect to (a) geography, (b) morphology, (c) salinity, (d) land-use. Panels: (a) West Sea (n = 186), South Sea (n =
105), and East Sea (n = 12). (b) Open coast (n = 173) and Embayment (n = 130). (c) Brackish (n = 101) and Saline (n = 202). (d) Agriculture/Beach (n = 248) and Industrial/Municipal
(n = 55). (e) Bare tidal flat (n = 171) and Salt marsh (n = 132). Relationships between organic carbon stocks and (f) human population (1 × 10,000), (g) tidal amplitude, and (h) mud
content of 303 core sediments of South Korea.

morphological settings could be a key factor to increase not only supply <63 μm) of bare tidal flats and salt marshes in different provinces
of waterborne sediment particles but also organic carbon burial in the were evaluated (Fig. 3). The analysis revealed that mud content had a
intertidal sediments (Collins et al., 2017). In the same context, we significantly positive correlation with organic carbon in bare tidal
found a positive relationship between mud content and organic carbon flats (r = 0.59, p < 0.01) and salt marshes (r = 0.30, p < 0.01) in
stock (r = 0.60, p < 0.01) (Fig. 2h). In other words, the larger surface all provinces (Fig. S6). The positive relationship between mud and
areas of more muddy sediment particles provide a better capture capac- organic carbon content has been repeatedly documented (Keil and
ity compared to sandy sediments (Keil and Hedges, 1993; Mayer, 1994; Hedges, 1993; Mayer, 1994; Bergamaschi et al., 1997; Flemming
Burdige, 2007; Serrano et al., 2016). and Delafontaine, 2000; Burdige, 2007; Serrano et al., 2016). This
relationship is attributed to the larger surface area of fine-grained
3.3. Effects of mud content and vegetation on sedimentary TOC sediments (e.g., mud) compared to coarse-grained sediments
(e.g., sand), providing more binding sites for sedimentary organic
Total organic carbon content and mud content in sediments varied carbon (Keil and Hedges, 1993; Mayer, 1994; Burdige, 2007;
in the bare tidal flats and salt marshes of the West, South, and East Serrano et al., 2016). Therefore, mud content could be used as a
Sea. We classified sediment textural type based on mud (silt + clay) universal proxy for estimating sedimentary organic carbon by
content; namely, sand (<25%), mixed (25–75%), and mud (>95% applying each relationship equation of bare tidal flats and salt
mud). The intertidal sediments collected in our study areas contained marshes in different provinces of South Korea.
both mixed and mud bottom fractions, with >25% mud content on av- Interestingly, significant differences in organic carbon content be-
erage, except for Nakdong River estuary and Uljin (Fig. S5). Gyeonggi tween bare tidal flats and salt marshes were detected in South Korea
had the highest mud content (mean ± SD, 80.2 ± 21.1%), followed by (p < 0.01) (Figs. 2e; S6). Salt marshes serve as highly efficient CO2
Southern Jeonnam (79.4 ± 27.3%), Chungnam (66.3 ± 27.2%), Western sinks through primary production and the trapping of sediments,
Jeonnam (61.0 ± 33.7%), Jeonbuk (51.0 ± 34.1%), Gyeongnam (26.3 ± resulting in their accreting higher sedimentary organic carbon com-
24.8%), and Gyeongbuk (0.6 ± 0.5%) (Fig. 3). In South Korea, tidal flats pared to bare tidal flats (Duarte et al., 2013; Spivak et al., 2019). Salt
are typically characterized by mud-dominated sediments in the upper marshes capture CO2 gas from the atmosphere, and then sequester car-
intertidal flats and sand-dominated sediments in the lower intertidal bon in organic forms within underlying sediments, living biomass
flats (Choi, 2014b). Moreover, textural trends in tidal flat sediments aboveground (leaves, stems) and belowground (roots), and non-living
are caused by differences to critical shear stress for deposition and ero- biomass (litter) (Mcleod et al., 2011). The structural complexity of veg-
sion (Dalrymple and Choi, 2003; Choi, 2014b) etated coastal ecosystems (root systems and dense vegetation) allows
As expected, organic carbon content was greater in mud-dominated salt marshes to be highly efficient in trapping sediment and associated
sediment (0.58 ± 0.24%) compared to mixed sediment (0.48 ± 0.28%) organic carbon originating from autochthonous and allochthonous
and sand-dominated sediment (0.23 ± 0.05). The relationships sources. Overall, higher sedimentary organic carbon content in salt
between sedimentary organic carbon and mud content (% particles marshes primarily results from higher carbon input through plant litter

6
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

Sand Mixed Mud Sand Mixed Mud Sand Mixed Mud Sand Mixed Mud
3 3
Gyeonggi Salt marsh Chungnam Salt marsh
Bare tidal flat Bare tidal flat
2 2
y = 0.007x - 0.093 y = 0.008x + 0.022 y = 0.001x + 0.226 y = 0.001x + 0.269
r = 0.61, p < 0.01 r = 0.45, p < 0.01 r = 0.15, p < 0.05 r = 0.08, p < 0.05
1 1

0 0
3 3
Jeonbuk Western Jeonnam

2 2
Organic carbon contents (%)

y = 0.003x + 0.05 y = 0.003x + 0.07 y = 0.001x + 0.195 y = 0.004x + 0.055


r = 0.73, p < 0.01 r = 0.64, p < 0.01 r = 0.33, p < 0.01 r = 0.38, p < 0.01
1 1

0 0
3 3
Southern Jeonnam Gyeongnam

2 2
y = 0.008x - 0.017 y = 0.008x + 0.286 y = 0.009x + 0.869 y = 0.013x + 0.131
r = 0.73, p < 0.01 r = 0.47, p < 0.01 r = 0.67, p < 0.01 r = 0.29, p < 0.01
1 1

0 0
3
Gyeongbuk Study areas in South Korea
2 West Sea Gyeonggi, Chungnam
Jeonbuk, Western Jeonnam
1 South Sea Southern Jeonnam, Gyeongnam
East Sea Gyeongbuk
0
0 20 40 60 80 100 0 20 40 60 80 100
Mud contents (%)

Fig. 3. Relationships between mud content and organic carbon content in the sediments of bare tidal flats and salt marshes in the provinces of Gyeonggi, Chungnam, Jeonbuk, Western
Jeonnam, Southern Jeonnam, Gyeongnam, and Gyeongbuk, South Korea. The textural type of sediment was classified into 3 types based on mud (silt + clay) contents: followed by
sand (<25% mud), mixed (25–75% mud), and mud (>75% mud) (Flemming, 2000).

and roots, and their being located in more saturated and, presumably, grid zones (Table S7). Through these comprehensive analyses, the cur-
more anaerobic environments (Yuan et al., 2015; Spivak et al., 2019). rent study reported tidal flat areas per sediment textural type along
the entire coast of the West, South, and East Sea of South Korea. The re-
3.4. Validation of tidal flat areas and sediment textural types using remote mote sensing results delineated three types of tidal flat areas based on
sensing classification sediment grain size: 1) mixed (mud dominant) tidal flats (Gyeonggi,
Chungnam, Western Jeonnam, Western Jeonnam, Southern Jeonnam,
The intertidal flats of the West, South, and East Sea were divided into Gyeongnam); 2) mixed (sand dominant) tidal flats (Incheon, Jeonbuk);
11,905 grid zones, with the tidal flat area being delineated using QGIS and 3) sandy tidal flats (Gyeongbuk, Ulsan, Gangwon). As a result,
(Figs. 4a; S1). The analysis showed that Incheon had the greatest tidal mixed tidal flats had the greatest areas in the southwestern coast of
flat area (742 km2), followed by Western Jeonnam (595 km2), Korea.
Chungnam (378 km2), Southern Jeonnam (281 km2), Gyeongnam
(265 km2), Gyeonggi (178 km2), Busan (31 km2), Jeonbuk (12 km2), 3.5. Estimation of organic carbon stocks and sequestration rates in South
Gyeongbuk (4 km2), Gangwon (2 km2), and Ulsan (2 km2) (Table 1). Korea
The textural type of sediments in all grid zones was classified by re-
motely sensed imagery as sand, mixed, and mud. Remote sensing and Through integrating sedimentary organic carbon stock per unit with
experimental data classifications were generally well matched. A signif- tidal flat type, we estimated the organic carbon stocks (Table S8) and
icant positive relationship was obtained for remote sensing classifica- sequestration rates (Table S9) in sand, mixed, and mud-dominated
tion and measured mud content (r = 0.40, p < 0.01) (Fig. 4b; c). In sediments. For tidal flats delineated by remote sensing, Gyeonggi
parallel to determining sediment textural type, we delineated each (including Incheon) had the highest organic carbon stocks
tidal flat area as sand, mixed, and mud-dominated sediments in all (6,167,559 Mg C), followed by Gyeongnam (including Busan)

7
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

(a) Satellite imagery

(a’)
30
Incheon Gangwon
(n = 262)
Gyeonggi
(n = 2,775)
Chungnam
(n = 1,446)
South Korea
West Chungnam (n = 11,905)
(n = 1,446)
Tidal flat area Sea Gyeongbuk
~368 km2
~300 (n = 364)

(a’) Jeonbuk
Ulsan

(n = 821)
Gyeongnam Busan
(n = 1,425)
Seosan
Western Jeonnam East
Garolim
(n = 2,756) Sea
Bay Southern Jeonnam
(n = 2,056)

Taean South
N Sea
Grid (0.9 x 0.9 km) 50 km

(b) (c)
100

Mud
(n = 34)
Mud

0 10 24
Experimental classification

80
Mud content (%)

60 r = 0.40, p < 0.01


(n = 34)

Mixed
Mixed

2 22 10
40
(n = 6)
Sand

20
4 2 0

Sand
0
Sand Mixed Mud Sand Mixed Mud
(n = 6) (n = 34) (n = 34) (n = 5) (n = 34) (n = 34)

Remote sensing classification Remote sensing classification


Fig. 4. Map showing 11,905 grid zones classified by remote sensing algorithms along the west, south, and east coasts of South Korea. (a) Grid zones (n = 1,446) of tidal flat areas
(~368 km2) in Chungnam Province. (a′) Magnified satellite image of tidal flats along the Garolim Bay. All satellite images were obtained from Bing Map. (b) Relationship between remote
sensing classification and mud content of core sediments at the sampling sites.

(2,089,279 Mg C), Western Jeonnam (1,952,907 Mg C), Southern We conducted an extensive literature review of data on carbon that
Jeonnam (1,621,985 Mg C), Chungnam (1,274,415 Mg C), Jeonbuk were available for salt marshes and bare tidal flats in the Yellow Sea
(20,211 Mg C), Gyeongbuk (including Ulsan) (11,433 Mg C), and of China (Table S11). Organic carbon stocks in the sediments of
Gangwon (4,361 Mg C) (Table 1; Fig. 5). The organic carbon sequestra- China's coastal areas were available from the published literature,
tion rate of all provinces in South Korea was also estimated from sedi- encompassing typical bare intertidal flats and salt marsh zones along
mentation rates. The results provided baseline values for organic the Yellow Sea, including the Liaohe Delta, Liaodong, Dongying Port,
carbon stocks (Total: 13,142,149 Mg C) and sequestration rates Shandong, Yellow River Estuary, Yancheng Jiangsu, Sheyang, Jiangsu,
(71,383 Mg C yr−1; ~262,000 Mg CO2 eq. yr−1) in the tidal flats of Wanggang River estuary, Jiangsu, Chongming Island, and Shanghai.
Korea. Total organic carbon content was positively correlated with Sediment depth for the reported organic carbon stocks ranged from
mud content; thus, organic carbon stock was also higher in mud- 10 to 100 cm across studies; thus, organic carbon stocks were normal-
dominated sediments (Table S10). However, current estimate of organic ized to the amount within 1 m depth for all subsequent calculations.
carbon stocks and sequestration rates was based on tidal flat delineated The results showed that, for China, organic carbon stocks ranged from
data, with no separation of bare tidal flats or salt marshes in the study 3 to 116 Mg C ha−1 in bare tidal flats and 4 to 170 Mg C ha−1 in salt
area. Thus, further study is required. marshes (Table S11). For South Korea, organic carbon stocks ranged

8
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

Table 1 halophyte habitats in China and Korea were evaluated cautiously. In


Organic carbon stock (Mg C) and organic carbon sequestration rate (Mg C yr−1) in the China, three species of halophytes (Phragmites sp., Spartina sp., and
coastal regions along the west, south, and east coast of South Korea (1 Mg = 106 g).
Suaeda sp.) dominate the vegetation in intertidal flats. In comparison,
Sea Region Tidal Sedimentation Oraganic Organic Phragmites sp. and Suaeda sp. are the dominant halophytes in most
flat rate (cm yr−1) carbon stock carbon coastal areas of South Korea, while Spartina sp. habitats are only found
area (Mg C) sequestration
This Reference in Ganghwa of Gyeonggi (Table S3). Yuan et al. (2015) reported that
(km2) rate (Mg C
study sedimentary organic carbon sequestration rates in S. alterniflora
yr−1)
marshes were 2.63 to 8.78 times higher compared to those of native hal-
West Sea Incheon 742 0.69 4,923,784 34,425
Gyeonggi 178 0.72 1,243,775 9,048 ophyte marshes (e.g., Phragmites australis and Suaeda salsa) in
Chungnam 378 0.41 1,274,415 5,240 Yancheng National Nature Reserve, China. Therefore, the species com-
Jeonbuk 12 0.49 20,211 100 position of halophytes contributes to different burial rates of organic
Jeonnam 595 0.40 1,952,907 7,886 carbon in intertidal flats.
Subtotal 1,906 9,415,091 56,698
South Sea Jeonnam 281 0.38 1,621,985 6,198
Only a small number of studies exist on organic carbon stocks and
Gyeongnam 265 0.41b 1,939,344 7,979 sequestration rates in bare tidal flats areas (Chen et al., 2020). Bare
Busan 31 0.30c 149,935 451 tidal flats have relatively small amounts of organic carbon stocks, due
Subtotal 577 3,711,264 14,629 to their having low net primary production (NPP) compared to salt
East Sea Gangwon 2a 0.33d 4,361 14
marshes, seagrasses, and mangroves (Table S12). Nevertheless, given
Gyeongbuk 4a 0.27e 8,009 22
Ulsan 2a 0.60f 3,424 21 extensive areal coverage and microphytobenthos, bare tidal flats could
Subtotal 9a 15,794 57 be an important carbon sink (Chen et al., 2020; Lin et al., 2020), and
Total 2,491 13,142,149 71,383 also a terminal reservoir of detrital organic matter from adjacent
a
Tidal flat areas were delineated using Electronic Navigational Chart (ENC) data. “Green Carbon” ecosystems.
b
Park and Lee (1996); Woo et al. (2003); Jeong et al. (2006); Lim et al. (2012).
c
Cho et al. (2000). 4. Conclusions
d
Song et al. (2019).
e
Park et al. (1999).
f
Cha et al. (2005). The present study demonstrated the distribution of organic carbon
stocks and sequestration rates of coastal sediments along the west,
south, and east coasts of Korea. This study is the first to document the
from 1 to 145 Mg C ha−1 in bare tidal flats and 4 to 161 Mg C ha−1 in salt organic carbon stocks and sequestration rates in the Korean tidal flats,
marshes. Among the two countries, Chinese salt marshes generally had at the national scale, based on the extensive field surveys combined
higher organic carbon stocks than Korean salt marshes. Thus, the differ- with state of the art remote sensing technology. The results showed
ent rates of increase for organic carbon stocks in the sediment of that major variation exists with respect to spatio-physiographic

(a) (a) (h) (h)


Gangwon
Gyeonggi Gyeonggi
(920 km2)
(b) (g)
Gangwon
(2 km2)
Chungnam South
20 Km
Korea Gyeongbuk 30 Km
49% 29% 21% 100%
(c)
(b) Jeonbuk (g)
Gyeongnam
(d) Western Gyeongbuk
Chungnam Jeonnam
(6 km2)
(378 km2) Southern
Jeonnam (f)
20 Km (e) 40 Km
42% 38% 20% 50 km 100%

(c) (d) (e) Southtern (f) Gyeongnam


Western Jeonnam (296 km2)
Jeonnam 2
(281 km )
(595 km2)
Jeonbuk
(12 km2)

10 Km 35 Km 35 Km 20 Km
72% 13%14%
13% 14% 26% 40% 33% 11% 65% 24% 17% 59% 23%

Organic carbon stocks (103 Mg) Sediment types Organic carbon stocks (Mg) Organic carbon sequestration (Mg yr-1)

0 2 4 6 Sand Mixed Mud 1,000 x 103 Mg 5 x 103 Mg yr-1

Fig. 5. Organic carbon stocks, organic carbon sequestration rates, and sediment textural types (sand, mixed, mud) at the provinces of: (a) Gyeonggi, (b) Chungnam, (c) Jeonbuk,
(d) Western Jeonnam, (e) Southern Jeonnam, (f) Gyeongnam, (g) Gyeongbuk, and (h) Gangwon, South Korea.

9
J. Lee, B. Kim, J. Noh et al. Science of the Total Environment 793 (2021) 148568

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