Journal of Environmental Protection, 2011, 2, 1285-1294
doi :1 0.4236/ jep.2011. 210148 Published Online December 2011 (http://www.SciRP.org/journal/jep)
1285
Characteristics of Large-Scale Harmful Algal
Blooms (HABs) in the Yangtze River Estuary and
the Adjacent East China Sea (ECS)
from 2000 to 2010
Li Shen1*, Huiping Xu1, Xulin Guo2, Meng Li2
1State Key Laboratory of Marine Geology, Tongji University, Shanghai, China; 2Department of Geography and Planning, University
of Saskatchewan, Saskatoon, Canada.
Received S eptember 9th, 2011; revised October 12th, 2011; accepted November 17th, 2011.
ABSTRACT
Harmful algal blooms (HABs) are a serious worldwide issue which has posed great risks on marine ecosystems and
public health by directly releasing toxins or indirectly leading to anoxia in marine environment. In recent years HABs
have caused huge economic losses in China, particularly in the Yangtze Estuary and the adjacent East China Sea (ECS).
The present study investigated the spatial-temporal and species characteristics of large-scale HABs in this area using
geographic information system (GIS) Kernel Density Estimation (KDE) spatial analysis, statistical methods and sa-
tellite image interpretation. Results revealed that the Yangtze Estuary, Zhoushan island, Xiangshan bay and Jiushan
island are the regions with highest frequency of large-scale HABs. HABs in the ECS reached a peak in terms of total
number and area in 2003 to 2005 and occupied a high percentage (around 70% in area and 60% in occurrence) in the
four Chinese coastal waters. The number of large-scale HABs (>1000 km2) in the Yangtze Estuary and the adjacent
ECS declined after 2005 while that of HABs (>100 km2) declined after 2008. Large-scale HABs occurrences con-
centrated in summer (May to July), and the averaged duration increased continually from the shortest time (1.3 days) in
2001 to the longest (10.9 days) in 2010 for each HAB. 17 causative species were found with Prorocentrum dentutam as
the most frequent dominant species, followed by Skeletonema costatum, Karenia mikimotoi, and Chaetoceros curvisetus.
Water discoloration observed in MODIS satellite true color images was well consistent with the corresponding HABs
reported by State Oceanic Administration of China (SOA). Multiple factors involving eutrophication, physical dynamics,
topography and deposition conditions contributed to the formation of frequent HABs in the ECS. Three strategies
including establishing a synthesized system, improving the previous database and investigating multiple contributors
were proposed for future HABs monitoring and management.
Keywords: Harmful Algal Blooms (HABs), Yangtze Estuary, The East China Sea, Spatial and Temporal Characteristics,
Causative Species, Remote Sensing
1. Introduction
Harmful algal blooms (HABs), also known as “red tides”,
have become a serious environmental issue which draws
great attention in both governments and academic com-
munities worldwide. Especially in recent years most coas-
tal areas around the world are severely suffering from
HABs of increasing frequency and expanding spatial ex-
tent [1,2]. HAB phytoplankton species can cause damage
to marine ecosystems as well as public health in two ways.
One is to directly release toxins and the other is to induce
hypoxia and anoxia of marine organisms by accumu-
lating biomass [3,4]. HABs are considered as one of the
biggest marine disasters due to the considerable environ-
mental contamination and huge economic losses as a re-
sult of mass morality of aquaculture [5,6].
China is a country with board coastal areas contributed
by four marginal seas namely Bohai, Yello w Sea, the East
China Sea (ECS) and the South China Sea, have been post
great risk by HABs ever y year since the first d ocum ented
HAB in 1933 [2,7]. According to previous investigation,
the ECS, consisting of broad waters (the Yangtze Estuary,

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1286 China Sea (ECS) from 2000 to 2010
the coastal areas of Zhejiang and Fujian province), is the
area most rigorously impacted by HABs among the four
main coastal waters nationwide. In particular, the Yangt-
ze River and the coast of Zhejiang Province are the hots-
pots of frequent large-scale and intensive HABs in the
ECS [7-9]. Economic developments facilitated by aqua-
culture industries and coastal recreations of Shanghai (the
number one metropolis in China) and Zhejiang Province
(the most developed region in China) are threatened by
annual HAB occurrences in the aforementioned areas.
Worse still, Chen et al. [10] pointed out that those HABs
in the ECS if last for more than 3 weeks might be trans-
ported to the Japanese or Korean coast by Kuroshio to
cause worldwide harm. Therefore, studying the HABs
trends in t he EC S with reg ard s to the spat ial -te mpor al c ha-
racteristics is of great significance for forecasting marine
damage, protecting pu blic health as well as promoting eco-
nomic development not only in China but also in other
neighboring count ries.
In the present study we analyzed the spatial and tem-
poral variability of historical large-scale HAB events
from 2000 to 2010 in the Yangtze Estuary and the adja-
cent ECS water using GIS techniques and statistical me-
thods. We also used MODIS satellite data to show the
potentiality of obs ervi ng larg e- scale HA Bs in th e tru e com-
posite imagery derived from basic remote sensing pro-
cessing and interpretation. In addition, the contributing fac-
tors for frequent HABs and potential strategies for mo-
nitor ring such HABs are also discussed.
2. Materials and Methods
2.1. Study Area
Our study area is the ECS specifically in the Yangtze
River Estuary and the adjacent water (around 27˚ - 32˚N,
120˚ - 123˚E) shown in Figure 1. As a marginal sea, the
ECS lying between the Asia Continent and the Pacific
Ocean, has broad water with a variety of islands (Hua-
niao shan, Ma’an, Shengsi, Zhoushan, Jiushan, Yushan,
Dong ji, Dongtou and Nanlu). The complicated oceano-
graphic characteristics in this region are contributed by
the interaction of complex circulation systems, meteoro-
logical conditions as well as geological topography. This
area is also characterized by high entrophication and pri-
mary productivity from various nutrition sources such as
the runoff of the Yangtze River and the coastal subsur-
face water [11]. This area with the largest fishery in
Zhoushan and Shengsi islands plays an important role in
the local and national economical growth but at the same
time suffers from serious HABs every year. Locations of
Figure 1. The study area and locations of historical frequent HABs (alphabetically marked). A. (the Yangtze Estuary), B.
(Huaniao shan island), C. (Ma’an island), D. (Shengsi island), E. (Hangzhou bay), F. (Zhoushan island), G. (Xiangshan bay),
. (Jiushan island), I. (Yushan island), J. (Yushan island), K. (Dongtou island), L. (Cangnan areas), and M. (Nanlu island). H

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1287
China Sea (ECS) from 2000 to 2010
historical frequent HABs are alphabetically marked in Fi-
gure 1.
2.2. Data
We have collected a total of 84 large-scale HABs events
(coverage > 100 km2) in the study area for the past 11
years (2000-2010) from annually reported bulletins in-
cluding the China Marine Environmental Quality Bulle-
tin, the China Marine Disasters Bulletin and the Shanghai
Marine Envir onmental Q ualit y Bulleti n by the St ate Ocea -
nic Administration of China (SOA) [12-14]. Those data
was obtained from the HAB database established by pre-
vious research projects conducted in the 11 HAB moni-
toring stations which were set up in the ECS by the SOA
[7]. More detail information including the start-end time,
locations, areas, causative species, as well as cell concen-
trations of each HAB event can be provided through
ship-tracking surveys, autonomous moorings and volun-
teer’s investigation [15].
Moderate Resolution Imaging Spectrometer (MODIS)
L1B satellite data was used to demonstrate large-scale
HABs at a broad spatial scope from space. MODIS is a
remote sensor with 36 spectral bands (0.405 to14.385 µm)
at three spatial resolutions (250 m, 500 m, and 1000 m),
and it can view the entire earth surface every 1 or 2 days.
The advantages in spectral, temporal and spatial resolu-
tions of satellite imagery can lead to more efficiency in
large-scale HABs monitoring. We obtained those data
from NASA at LAADS Web (http://ladsweb.nascom.
nasa.gov/).
2.3. Spatial Analysis of HABs
Geographical information system (GIS) spatial analyst
method was applied to conduct the spatial pattern analy-
sis for the eleven-year (2000 to 2010) large-scale HAB
events (>100 km2) in the Yangtze Estuary and the adja-
cent ECS. ArcGIS (10.0 version) was the platform to
perform the analysis. Overlaid on a basemap of the ECS,
a new point shapefile layer was created to exhibit those
HAB events with the relative information stored in an
attribute table. Each HAB event was represented by a
central point of the polygon shape of the actual HAB
coverage. Wang and Wu [2] suggested using this point
pattern due to the difficulty of measuring the exact ir-
regular and variable shape of a HAB coverage. Besides,
they also pointed out that GIS techniques have more ad-
vantages in point pattern analysis than in polygons. The
geographic coordinate was determined according to the
location information of each HAB event provided by the
SOA. And the projection of these HAB points was as-
signed GSC-WGS-1984 consistent with the coordinate
system of the basemap. The geographical boundary of the
spatial analysis is set according to the extent of our study
area.
The frequency of HAB occurrences can be obtained
from the degree of point concentration on a continuous
density surface created by Kernel Density Estimation
(KDE). KDE is a spatial analysis method with a kernel
defined by a circle in a certain radius moving across the
study area. The distance from the centre of the circle to
the HAB point is measured to give the weight for that
HAB event and to determine the density for the centre
point [16].
2.4. Temporal Analysis of HABs
We analyzed the total occurrence and area of HABs in
the ESC in each year from 2000 to 2010 as well as its
percentage of the summed HAB events among all the
four Chinese coastal waters. In the Yangtze Estuary and
the adjacent ECS water, we mainly focus on large-scale
HABs with an area over 100 km2. T he co ve ra ge va r iatio n
of large-scale HABs at two levels (>100 km2 and >1000
km2) in our study area from 2000 to 2010 was investi-
gated. We have also compared occurrences in three dif-
ferent periods (spring, summer, and autumn) to under-
stand the seasonality pattern of large-scale HABs (>100
km2). In addition, the average duration for HABs (>100
km2) in each year was extracted from the time data of
each HAB event. We also investigated the causative spe-
cies of large-scale HABs (>100 km2) in the past 11 years
and ranked them in terms of HAB occurrences and area.
2.5. Detection of Satellite Imagery
Water discoloratio n observed in the satellite ima gery has
great possibility in indicating large-scale HAB events
and revealing their location and size information [8,17].
Here we selected 3 relatively cloud-free scenes of MO-
DIS L1B data to demonstrate this application. The origi-
nal data was preprocessed by implementing radiometric
and geometric corrections to derive reflectance values.
Then three spectral bands 645 nm (Red), 555 nm (Green)
and 465 nm (Blue) were combined into one true color
composite image which can reflect the real information
of earth surface. Equalization enhancement method was
used to improve the clearance of the images for better
interpretation. Admittedly, not all HABs can be distin-
guished from neighboring water due to their inconspicu-
ous anomaly; however, visual interpretation can still be
an easy and necessary procedure to avoid missing any
occurrence sign of HAB events.
3. Results and Discussions
3.1. Spatial Characteristics of HABs
Figure 2 shows the spatial distribution of large-scale

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1288 China Sea (ECS) from 2000 to 2010
Figure 2. Locations of large-scale HABs (>100 km2) in periods from 2000 to 2010 in the Yangtze Estuary and the adjacent
ECS water. Each point represents one HAB event.
HABs (100 km2) in the study area from 2000 to 2010. In
general, they widely dispersed in all coastal waters of
Shanghai municipality as well as Zhejiang province, and
clustered in some certain areas. The KDE result (Figure
3) showed that the Yangtze Estuary (A), Zhoushan island
(F), Xiangshan bay (G) and Jiushan island (H) are the
regions with highest frequenc y of large-scale HABs, and
these regions are also hotspots of HABs at normal scales
in the ECS along isobaths of 30 - 60 m in the ECS [2,7].
High frequency of large-scale HABs appeared in around
20 km scope outside of the HAB hotspots, and areas of
medium frequency were observed in regions of another
20 km away. Other areas have comparatively low possi-
bility to induce large-scale HABs
3.2. Temporal Characteristics of HABs
Both occurrences and areas of HABs in the ECS were
found to be sharply increasing in the early years of the
past 11 years from 2000 to 2010 until a peak appears
(2003 for occurrences and 2005 for areas), and then show-
ed a decreasing pattern in the rest years (Figure 4(a)).
Particularly in 2004 and 2006, HAB occurrences and
areas appeared contrast variation characterist ics (lo w HAB
occurrence with high bloom area), indicating that the scale
of these HABs are large enough to cover a huge area in
despite of a small number of occurrences. After 2006, the
scale of HABs in the ECS became smaller which can be
found in Figure 4(a). Figure 4(b) shows that HABs in
the ECS accounted for a high percentage of the total
HABs in the all four Chinese coastal water in terms of
occurrence number and areas, especially in 2002 (64.6%
for occurrence and 88.7% for area), 2003 (72.3% for
occurrence and 89.3% for area) and 2008 (69.6% for
occurrence and 88% for area).
In the Yangtze Estuary and the adjacent ECS water,
number of HABs with an area over 1000 km2 has an in-
creasing trend from 2000 to 2005, but declined in the
next ha lf of the se 1 1 years ( blue hi sto gra ms in Figure 5).
In 2005 alone, the occurrences of such large-scale HABs
were found to reach 8. Red histograms in Figure 5 illus-
trated occurrences of HABs over 100 km2 kept rising
until 2008 with a peak of 16, and in the last two years
decreased but still maintained at a higher lever (over 9).
We also investigated the seasonality and duration of
large-scale HABs (>100 km2) in this area. The hotspot
season of HABs was observed in Figure 6 to fall in sum-
mer (May-July) with an annually averaged occurrence of
6.27, and a total number of 66 responsible for 78.4% of
the documented 88 HABs from 2000 to 2010. Prior to
2007, only one large-scale HAB (>100 km2) event was
reported in autumn (August to October) but later than
007 12 HABs (>100 km2) were recorded in autumn. In 2

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1289
China Sea (ECS) from 2000 to 2010
Figure 3. Kernel Density Estimation (KDE) result conducted by GIS spatial analyst for large-scale HABs frequency in the
study area from 2000 to 2010. Four categories of HAB frequency were obtained.
spring (February to April) large-scale HABs were sel-
domly found with an annually averaged number of 0.45
(Figure 6). The averaged duration for large-scale HABs
(>100 km2) are found to grow continually with a few
slight fluctuation. The shortest time of a HAB was 1.3
days in 2001 and the longest achieved 10.9 days in 2010
(Figure 7).
3.3. Variation of Causative Species
17 causative species of large-scale HABs (>100 km2)
inthe Yangtze Estuary and the adjacent ECS from 2000
to 2010 were listed in Tab le 1 . Most species can be iden-
tified to known species while so me were named at family
or genus level. Prorocentrum dentutam was ranked num-
ber one dominant species occupying 42 events with a
total area of 46,510 km2, followed by Skeletonema co-
statum dominating 29 HAB events with an area of 23,110
km2, Karenia mikimotoi with 12 occurrences and 20,260
km2, and Chaetoceros curvisetus with 9 occurrences and
3600 km2. Among them, Karenia mikimotoi, a toxin-
releasing species, was firstly found in 2004 in the ECS,
and then caused more intensive HABs in later years [2].
Prorocentrum dentutam and Skeletonema costatum are
non-toxin species but can accumulate biomass to cause
hypoxia and anoxia of the marine environment. Chen et
al. [10] concluded that Prorocentrum dentutam had taken
the place of Skeletonema costatum to become the top one
Table 1. T a ble t ype st yles (Table caption is i ndispens able).
Cau sative Species Occurrences Areas (km2)
Prorocentrum dentutam 42 46,510
Skele t on ema cost at um 20 23,110
Kare nia mikimo toi 12 20,260
Chae to c eros cur visetus 9 3600
Mesodinium rubrum 4 1910
Scrippsiella trochoidea 4 3900
Thalassiosira sp. 3 8400
Pseudo-nitizschia pungens 3 800
Ceratium fusus 2 620
Noctiluca sc intillans 2 1500
Prorocentrum triestinum 2 3400
Gymnodinium sp. 1 3000
Microalgae 1 100
Gonyaulax spinife ra 1 300
Chaetoceros compress us 1 700
Ceratium furca 1 100
Leptocyli ndrus dan icus 1 100

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1290 China Sea (ECS) from 2000 to 2010
(a)
(b)
Figure 4. HAB occurrences and areas in the ECS from 2000 to 2010. (a) Total number and area of annual HABs. (b) Per-
centage of HAB s (ECS) of the all four Chinese co astal areas.
HAB causative species in the ECS. One Prorocentrum
dentutam HAB was observe d covering an area over 10,000
km2 in 2004. Ot her phytoplankton species seldomly ca used
large-scale HABs by itself but in a seconddary role coo-
per ating w ith th e dom inan t speci es .
3.4. Observation of HABs in Satellite
MODIS true color composite images (Figure 8(a-c))
showed the water discoloration of two large-scale HABs
in May to June, 2005. According to the recorded HAB in-
formation provided by the SOA, a HAB with the cov-
erage of 7000 km2 caused by Prorocentrum dentutam and
Karenia mikimotoi occurred in the Yangtze Estuary from
May 24, 2005 to June 1, 2005. In the same year, another
large-scale HAB over 400 km2 caused by Skeletonema
costatum was also found in the Yangtze Estuary with cell
concentration of 4.2 × 107/L from June 15, to June 21
[12-14]. The areas circled in a highlighted red box were
the anomalies caused by the accumulated biomass of the
HAB phytoplankton, in notable contrast with the neigh-
boring waters. The locations of these discolored areas
were confirmed by the distribution information of the
corresponding HABs reported by the SOA. Those ab-
normal regions are well consistent with the areas of fre-

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1291
China Sea (ECS) from 2000 to 2010
Figure 5. Occurrences of large-scale HABs at two levels (>
100 km2 and >1000 km2) in the Yangtze Estuary and the ad-
jacent ECS from 2000 to 2010.
Figure 6. Seasonal occurrences of large-scale HABs (>100
km2) in th e Yangtze Estua r y and t he ad jac en t ECS from 2000
to 2010.
Figure 7. Annually averaged duration of each large-scale
HAB (>100 km2) event in the Yangtze Estuary and the ad-
jacent ECS from 2000 to 2010.
quent HABs in the ECS.
3.5. Contributing Factors for Large-Scale HABs
Multiple contributing factors can lead to the formation of
large-scale HABs in the study area. The severe eutrophi-
(a)
(b)
(c)
Figure 8. Water discoloration of HABs in MODIS true co-
lor composite images. (a). MODIS true color i mage on May
25, 2005; (b). MODIS true color image on May 29, 2005; (c).
MODIS true color image on June 16, 2005.
cation along with high productivity in the ECS was
thought to be the main inducement of frequent HABs by

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1292 China Sea (ECS) from 2000 to 2010
influencing the congregation rate of phytoplankton spe-
cies [18]. An extremely high cell concentration of phyto-
plankton species resulted from exponential propagation
can indicate a corresponding HAB [19]. The cell concen-
tration peak in the ECS normally appears in June to Sep-
tember such as Skeletonema costatum with average abun-
dance of 7.93 × 104 cell L–1 [20]. Increasing amounts of
nutrie nts fr om t he Ya ngtze Ri ver r unoff went to the EC S
every year, which provided necessary phosphorus and
nitrogen concentration to flourish HAB species [21]. An-
thropogenic effects such as overuse of fertilizers, in- dus-
trial sewage and excess fishery in the coastal cities (e.g.
Shanghai, Hangzhou and Ningbo) also play an impor-
tant role in leading to the eutrophication condition [20,22].
Besides, our study area is impacted by complicated
oceanographic processes and dynamics involving Taiwan
Warm Current (16˚C to 29.5˚C), the Yangtze Diluted
Water (>22˚C), the Yellow Sea Cold Current, the Ku-
roshio Current and the Zhejiang Coastal Current, which
can bring tremendous amounts of nutrients from different
sources. Particularly the Yangtze Diluted Water serves as
the main nutrient source because of the high suspended
sediment deposition in the area of west 122.5˚E. A con-
vergence zone characterized by the temperature and sa-
linity fonts is formed also around 122.5˚E where the Tai-
wan Warm Current meets with the nutrient-rich Yangtze
River, favorable for the formation of HABs. The north-
ward advection of the Taiwan Warm Current also plays a
signi ficant role to transp ort nutrien ts from a remote so urce
in Taiwan Strait. Meanwhil e, the Zhejiang Coastal C u r r e nt
can bring nutrients up to the HAB region from the sub-
surface layer in the upwelling zones [7,8,11,23,24].
Thirdly, our study area, on the northwest continental
shelf of the ECS, is characterized by special topography
and sediment deposition favorable for the HAB occur-
rences. The west slope of 6 × 10–3 in the de ep tr ough has
positive effects on the formation of upwelling currents
[25,26]. The large-scale HABs locate in the high-velocity
deposition zone in which nutrients at the bottom sedi-
ments can facilitate the implantation of algal cyst hy-
popus by the resuspending process particularly in sum-
mer [26,27]. That can explain why summer is the peak
period for frequent large-scale HABs [28].
3.6. Strategies for HABs Monitoring and
Management
For future monitoring and management of large-scale
HABs, there are some points that should be taken into
consideration. First, it is necessary to establish a synthe-
sized HAB system in the areas of frequent large-scale
HABs by combining multiple data sources including sa-
tellite remote sensing, aerial photography, in situ ship-
tracking surveys, autonomous moorings, and laboratory
analysis into a whole database. Particularly remote sens-
ing techniques are promising to conduct comprehensive
HAB research at different spatial and temporal scales.
Multiple satellite imagery can be fully utilized to extract
water classification and biophysical parameters distri-
bution for monitoring and forecasting HABs. Second, it
is of great help to enhance the previous HAB database by
investigating the spatial-temporal pattern of historical
large-scale HABs caused by different phytoplankton
species in a long period. In addition, multiple contri-
buting factors in biochemistry, physical dynamics, geo-
logy and meteorology should be comprehensively studied
for better understanding the true mechanism the large-scale
HABs .
4. Conclusions
The results in the present study show that from 2000 to
2010 the Yangtze Estuary, Zhoushan island, Xiangshan
bay and Jiushan island are the regions with highest fre-
quency of large-scale HAB. HABs in the ECS reached a
peak in terms of total number and total area in 2003 to
2005 and occupied a high percentage of HABs in the four
Chinese coastal waters. Number of large-scale HABs (>
1000 km2) in the Yangtze Estuary and the adjacent ECS
declined after 2005 while that of HABs (>100 km2)
declined after 2008. Large-scale HABs occurrences con-
centrated in summer (May to July) accounted for 78.4%
of the total HABs in the past 11 years. The averaged
duration for HABs (>100 km2) increased continually
with the shortest time (1.3) days in 2001 and the longest
(10.9 days) in 2010. In the study area 17 causative spe-
cies were found for those large-scale HABs (>100 km2)
with Prorocentrum dentutam as the most frequent domi-
nant species, followed by Skeletonema costatum, Kare-
nia mikimotoi, and Chaetoceros curvisetus from 2000 to
2010. Water discoloration found in satellite true color
composite imagery was well consistent with distributions
of the corresponding HABs in 2005 reported by SOA,
falli n g i n the r e gions of fr e quent H AB s d er i ved fr o m GI S
spatial analyst. Multiple factors involving eutrophication,
physical dynamics, topography and deposition conditions
can explain the formation of such large-scale HABs in
the ECS. Three strategies including establishing a syn-
thesized system, improving the previous database and in-
vestting multiple contributors were proposed for future
HABs monitoring and management.
5. Acknowledgements
This research was supported by the program of Key La-
boratory of Marine Geology in Tongji University under
number MG20080104 and Foundation of Shanghai Science
and Technology Committee on Key Projects und er nu mb e r

Characteristi cs of Large-Scale Harmful Algal Blooms (HABs) in t he Yangtze River Estuary and th e Adjacent E ast 1293
China Sea (ECS) from 2000 to 2010
09DZ1201000. The authors also would like to acknow-
ledge the reviewers for their comments and suggestions
on this manuscript.
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