Limnol. Oceanogr., 55(1), 2010, 1–10
2010, by the American Society of Limnology and Oceanography, Inc.
E
A relationship between submarine groundwater-borne nutrients traced by Ra isotopes
and the intensity of dinoflagellate red-tides occurring in the southern sea of Korea
Yong-Woo Lee,a Guebuem Kim,a,* Weol-Ae Lim,b and Dong-Woon Hwangb
a School
of Earth & Environmental Sciences/RIO, Seoul National University, Seoul, Korea
Fisheries Research and Development Institute, Busan, Korea
b National
Abstract
We measured short-lived radium isotopes (223Ra and 224Ra), dissolved inorganic and organic nutrients, and
photosynthetic pigments during the summers of 2006 and 2007 in the southern sea of Korea, where harmful
dinoflagellate blooms occur every year. The Ra tracer measurements reveal that coastal groundwater, rather than
other sources previous suggested (i.e., Yangtze River diluted water or Kuroshio currents), is the main source of
nutrients that fuel red tides in this region. Although inorganic-nutrient levels are different for different regions
and different years, either dissolved inorganic nitrogen or phosphorus is depleted in the red-tide region. This
depletion is accompanied by highly elevated levels of dissolved organic nutrients, transformed from groundwaterborne dissolved inorganic nutrients either inside Yeoja Bay or in offshore red-tide areas, thereby creating
favorable conditions for the growth of dinoflagellates in competition with diatoms. The intensity of red tides
correlates well with the activity of 224Ra (half life 5 3.66 d) in seawater over daily or yearly time scales. Because
the chemically conservative 224Ra can trace groundwater-borne nutrients, which are utilized by marine biota in
this red-tide region, the intensity of red tides seems to be related to the amount of nutrient-enriched groundwater
supplied to the offshore red-tide region.
effects on fin-fish farms over a large area from late summer
to early autumn. Dinoflagellate red-tide outbreaks occur at
offshore areas in the study region, although red tides
generally occur in coastal waters where large quantities of
inorganic nutrients are introduced from industrial, agricultural, and domestic effluents (Kang et al. 2002). Previous
studies have suggested that red tides in this region are
associated with the approach of the Yangtze River Diluted
Water (YRDW; Yang et al. 2000) or the oligotrophic
Kuroshio Warm Current ([KWC] Yang et al. 2000; Choi
2001; Lee 2008). Some other studies have suggested that the
breakdown of water-column stratification could be an
important factor triggering red-tide outbreaks in this region
(Choi 2001; Kang et al. 2002; Lee 2008).
However, Hwang et al. (2005a) and Lee and Kim (2007)
have identified the main source of nutrients that fuel red
tides in the study region as being SGD, rather than other
sources such as YRDW, KWC, or bottom waters. A series
of studies linking SGD and red-tide outbreaks occurring in
the southern sea of Korea is summarized in Table 1. In the
current study, we obtained more data in 2006 and 2007
when weak and intense red tides occurred, respectively.
These additional data sets have allowed us (1) to reconfirm
favorable conditions for the outbreak of red tides for
different years, (2) to link nutrient conditions driven by
SGD and daily changes in red-tide intensity, and (3) to link
levels of excess nutrient inputs traced by Ra isotopes and
yearly changes in red-tide intensity in the study region.
During the last few decades, the transport of landoriginated chemical species, including nutrients and pollutants, through submarine groundwater discharge (SGD),
has been proved to rival that through river runoffs (Burnett
et al. 2003; Kim et al. 2005; Swarzenski et al. 2006). Most of
the SGD-driven chemical flux studies, including the current
study, define SGD to consist of fresh groundwater,
recirculated seawater, or a composite of the two, and
recirculated seawater could contribute up to 90% of SGD
(Kim and Swarzenski in press). SGD-driven nutrients have
a significant effect on the primary production and
community composition of phytoplankton in coastal areas
(Lapointe 1997; LaRoche et al. 1997; Lee and Kim 2007).
Excess nutrient inputs through SGD often cause coastal
water eutrophication (Capone and Slater 1990; Valiela et
al. 1990; Charette et al. 2001), benthic macro-algal
eutrophication (Hwang et al. 2005b), dinoflagellate redtide outbreaks (Hwang et al. 2005a; Lee and Kim 2007),
brown-tide blooms in a Long Island embayment (Gobler
and Sañudo-Wilhelmy 2001), and harmful Karenia brevis
blooms off Florida (Hu et al. 2006). Although Gobler and
Sañudo-Wilhelmy (2001) showed statistically that temporal
variation in inorganic nutrient fluxes through SGD causes
brown-tide blooms in a Long Island embayment, the link
between SGD and red-tide outbreaks is still poorly
understood.
In this study region, off the southern coast of the Korean
peninsula, dinoflagellate (i.e., Cochlodinium polykrikoides)
red tides have occurred regularly since 1982 (Cho et al.
2001). The emergence of C. polykrikoides blooms has
increased in frequency, duration, and dimension since 1995
(Kim 1998). These dinoflagellate red tides have deleterious
* Corresponding
Methods
Study area and sampling—The study area is off the
southern coast of the Korean peninsula. Water in the area
flows northeastward, and it is a composite of Yellow Sea
seawater, oligotrophic Kuroshio water, and low-salinity
author: gkim@snu.ac.kr
1
2
Lee et al.
Table 1.
Study years
Summary of studies linking submarine groundwater discharge (SGD) and red tides in the southern sea of Korea.
Study areas
2003
Inside Yeoja Bay
2003
A fixed station off
Yeoja Bay
2002–2003
Inside Yeoja Bay–
Off Yeoja Bay
2006–2007
Off Yeoja Bay–
Tongyeong
Main findings
Submarine ‘‘brackish’’ groundwater discharge was estimated
to be 2.63107 m3 d21(87 m3 m22 yr21) in Yeoja Bay.
Submarine ‘‘brackish’’ groundwater was the main source
of DIN and DSi inside Yeoja Bay.
Real-time monitoring of biogeochemical parameters
displayed that the outbreak of dinoflagellate red tides
was associated with the limited growth of diatoms
under depleted DIP or DIN conditions.
SGD in Yeoja Bay provided inorganic nutrients for diatom
blooms. As water moved from Yeoja Bay to offshore
red-tide areas, inorganic nutrients decreased and organic
nutrients increased. Red tides broke out when either DIN
or DIP was depleted, while organic nutrients were enriched.
The previous findings on the sources of nutrients in the
red-tide areas and the conditions favorable for red-tide
outbreaks were reconfirmed. The daily or yearly variations
in intensity of red tides were related to the amount of
nutrient-enriched brackish groundwater supplied to the
offshore red-tide region.
YRDW during the summer–autumn seasons. Mean annual
precipitation is ,1500 mm, with most of rain falling during
the summer monsoon season. The spring tidal range is
,3.2 m. In general, the first bloom of dinoflagellate red
tides occurs off Oenarodo, and then propagates toward the
southeastern coast of Korea along the water current
(Fig. 1A,B). Yeoja Bay is relatively shallow (mean depth:
,5 m), with an area of ,320 km2.
In 2006, we collected surface-water samples for monitoring nutrients, Ra isotopes (223Ra and 224Ra), and
photosynthetic pigments in the coastal zone off Tongyeong
during 21–24 August (Fig. 1C). Water samples were
collected from shallow locations (water depth , 0.5 m)
using a submersible pump. Because the largest red tides
occurred in this region in 2002 and 2003 (Kim et al. 2004)
we attempted to monitor these parameters in order to link
SGD and red tides in this region. However, we did not
encounter red tides in this region in 2006.
In 2007, we reoccupied the area near Kuemhodo
(occupied in 2002 and 2003) between 17 and 25 August
(Fig. 1B). Significant red tides occurred there in 2007 (Bae
et al. 2008). For Sta. 1 and 2, we monitored the daily
variation in Ra and biogeochemical parameters. For other
stations, we collected one set of water samples for Ra and
biogeochemical parameters from visible red-tide patch
areas together with those from nonpatch areas for
comparison (Fig. 1B). In order to monitor the change in
Ra inside Yeoja Bay, which is the source region for the
discharge of groundwater-borne nutrients to the offshore
red-tide region (Hwang et al. 2005a), we measured 224Ra
and 223Ra activities in surface seawater near Yeoja Island,
at the center of Yeoja Bay (Fig. 1B). In addition, the survey
was conducted in coastal areas off Tongyeong (occupied in
2006) on 27 August 2007 (Fig. 1C). Brackish groundwater
samples were taken from nine shallow (, 0.5 m) and
deeper (, 10 m) wells around Yeoja Bay.
Reference
Hwang et al. 2005a
Kim et al. 2006
Lee and Kim 2007
This study
Measurements of Ra isotopes and biogeochemical parameters—The temperature and salinity of seawaters were
measured using a portable conductivity-temperature-depth
(CTD) probe (OceanSeven-302, Idronaut Srl.). Water
samples for nutrient analysis were filtered using a GF/F
filter (47-mm diameter) in the field, and then frozen until
z
{
3{
analysis. Nutrients (NO {
3 , NO 2 , NH 4 , PO 4 , and
Si(OH)4) were measured using an auto-analyzer (Futura
II+, Alliance Instruments). Dissolved inorganic nitrogen
z
{
(DIN) was calculated as the sum of NO {
3 , NO 2 , and NH 4 .
3{
We define dissolved inorganic phosphorus (DIP) as PO 4
and silicate (DSi) as Si(OH)4. Dissolved total nitrogen
(DTN) was measured using a Shimadzu TOC-VCPH/CPN
total carbon analyzer coupled to a nitrogen chemiluminescence detector. Dissolved organic nitrogen (DON) was
calculated by subtracting the concentration of DIN from
that of DTN. In order to analyze photosynthetic pigments of
phytoplankton, seawater samples were filtered using a GF/F
filter (47-mm diameter) in the field, and then stored in a deep
freezer (280uC) until analysis. Photosynthetic pigments were
measured by using a reverse-phase high-performance liquid
chromatograph (Waters Co. System) with a Rexchrom-S5100-ODS column (250 3 4.6 mm, particle size: 5 mm) after a
slight modification of the method of Wright et al. (1991).
For Ra analyses, seawater samples (,100 liters) were
collected in polypropylene cubitainers and then gravity-fed
through Mn-impregnated acrylic fibers at a flow rate of
min21. This flow rate ensures the quantitative adsorption of
Ra onto fibers (Kim et al. 2001). Upon returning to the lab,
the water content of Mn fibers was adjusted, and the activities
of 223Ra and 224Ra on Mn fibers were measured directly using
RaDeCC delayed-coincidence counting systems (Moore and
Arnold 1996; Kim et al. 2001). Uncertainties of Ra activities
are based on 1-sigma counting error propagations. The 224Ra
standard was inter-calibrated with a standard provided by
Florida State University (Dimova et al. 2008).
Groundwater-borne nutrients traced by Ra
3
Results
Fig. 1. Map showing (A) the location of the study area in the
southern sea of Korea, (B) seawater sampling stations off
Kuemhodo in 2007 (filled circles), and (C) seawater sampling
stations off Tongyeong in 2006 (filled circles) and 2007 (filled
triangles). A monitoring site is located at the center of Yeoja Bay
(filled triangles) in 2007. The open-circled stations are the centers
of the red-tide patches in 2007. Groundwater samples were
collected around Yeoja Bay (filled stars) in 2007.
During all study periods, temperature of surface water
ranged from 24.1uC to 30.4uC, which is favorable for the
growth of C. polykrikoides (Tables 2, 3). Salinity ranged
from 29.3 to 33.1 in 2006 and 2007 in both regions off
Kuemhodo and Tongyeong, which was slightly higher than
that in 2002 (27.6–31.1) and 2003 (27.8–30.2) off Kuemhodo (except for one station).
In the red-tide region off Kuemhodo, the concentrations
of DIN in seawater ranged from 0.45 to 19 (mean 5 3.5 6
4.9) mmol L21 in 2007, mostly lower than 2 mmol L21
(Table 2), which were generally lower than those of DON
(mean 5 5.9 6 3.1 mmol L21). In the red-tide region off
Tongyeong, the concentrations of DIN ranged from 2.7 to
8.1 (mean 5 4.9 6 2.4) mmol L21 in 2007, which were
slightly higher than those in 2006 (mean 5 2.9 6 0.4 mmol L21;
Table 3). The concentrations of DIN were ,690 6
460 mmol L21 (n 5 17) in coastal groundwater around Yeoja
Bay in 2007, which were one to two orders of magnitude higher
than those in seawater (Table 4). The concentrations of DON
were negligible compared with those of DIN in coastal
groundwater.
In all study stations off Kuemhodo, the concentrations
of DIP and DSi in seawater were lower than 0.15 mmol L21
and 2.5 mmol L21, respectively, except for some elevated
DSi stations in 2007. In the red-tide region off Tongyeong,
the concentrations of DIP in 2007 (mean 5 0.29 6
0.11 mmol L21) were higher than those in 2006 (mean 5
0.11 6 0.08 mmol L21), while the concentrations of DSi in
2007 (mean 5 1.9 6 0.8 mmol L21) were lower than those
in 2006 (mean 5 7.6 6 1.3 mmol L21).
In the red-tide region off Kuemhodo, the concentrations
of chlorophyll a (Chl a) in red-tide patch areas were ,3610
6 980 ng L21 in 2007, about a factor of four higher than
those in nonpatch areas (mean 5 860 6 480 ng L21;
Table 2). Similarly, the concentrations of peridinin, an
index of dinoflagellates, were ,5450 6 2470 ng L21 in
patch areas, an order of magnitude higher than those in
nonpatch areas (mean 5 480 6 730 ng L21). The concentrations of Chl a decreased from 17 August (5110 ng L21 to
3460 ng L21) to 25 August (1180 ng L21 to 240 ng L21) in
both red-tide patch and nonpatch areas. In the red-tide
region off Tongyeong, the concentration of Chl a was ,2320
6 1000 ng L21 in 2007, which was much higher than that in
2006 (mean 5 630 6 200 ng L21; Table 3).
The activities of Ra in seawater ranged from 0.17 Bq
m23 to 0.45 Bq m23 for 223Ra and from 1.14 Bq m23 to
4.98 Bq m23 for 224Ra in the dinoflagellate red-tide region
off Kuemhodo in 2007 (Table 2), which were much lower
than those in the monitoring site inside Yeoja Bay (0.67 6
0.11 Bq m23 for 223Ra and 7.62 6 1.12 Bq m23 for 224Ra;
Table 5). In coastal groundwater, average activities were
,6.4 6 5.9 Bq m23 for 223Ra and 114 6 103 Bq m23 for
224Ra (Table 4), which were an order of magnitude higher
than those in Yeoja Bay seawaters. In the study region off
Tongyeong, the activities of Ra were ,0.20 6 0.10 Bq m23
for 223Ra and 1.50 6 0.79 Bq m23 for 224Ra in 2007, which
were a factor of two lower than those in seawater off
Kuemhodo, but higher than those (0.08 6 0.04 Bq m23 for
4
Lee et al.
Table 2. Concentrations of Ra isotopes, nutrients, and photosynthetic pigments in surface seawaters outside Yeoja Bay in the
southern sea of Korea in 2007.
223Ra
Date
Sta.
17 Aug
1
2
P1
P2
P3
P4
1
2
P5
P6
P7
1
2
P8
P9
P10
1
2
P11
P12
20 Aug
23 Aug
25 Aug
*
{
{
1
Temp.
(uC) Salinity
25.4
26.4
26.3
24.1
24.5
24.8
27.3
27.8
26.4
28.0
28.1
27.1
26.9
27.3
27.5
27.5
28.8
28.2
26.4
28.3
224Ra
DIN*
DIP{
Bq m23
32.1
32.1
32.3
31.5
29.3
31.5
32.2
32.2
32.0
31.3
31.5
32.2
32.1
31.9
31.8
31.8
32.2
32.2
32.1
31.9
0.3360.07
0.3160.04
0.3460.04
0.2460.04
0.2260.05
0.3260.04
0.3560.04
0.4560.07
0.3560.03
0.3160.06
0.3260.07
0.1760.01
0.2160.02
0.2260.03
0.3060.03
0.3360.02
0.1960.02
0.1860.03
0.2360.03
0.2760.02
DSi{
DON1
Peridinin Fucoxanthin
mmol L21
4.7560.24
3.3160.10
3.9560.12
3.3260.12
2.3960.15
4.0260.11
3.5660.09
4.9860.19
3.8760.10
3.1960.16
3.5960.20
1.1460.04
1.5160.05
2.0260.08
2.2660.13
2.6860.06
1.9060.08
1.5460.08
2.0260.09
2.5660.05
1.62
3.14
1.37
11.5
1.61
1.87
0.79
0.88
1.33
0.57
0.98
0.77
0.55
0.58
0.45
1.13
19.4
4.08
6.09
10.7
0.03
0.00
0.05
0.00
0.01
0.06
0.04
0.04
0.05
0.06
0.09
0.11
0.10
0.11
0.12
0.14
0.10
0.10
0.13
0.12
2.45
0.28
5.12
0.01
0.01
2.49
2.06
2.49
0.64
0.86
0.44
4.40
2.22
1.16
1.53
1.42
1.18
2.51
0.97
0.29
Chl a
ng L21
5.37
10.1
6.04
2.39
5.46
8.95
5.55
5.68
9.24
7.19
3.64
11.6
4.68
6.77
5.95
6.12
0.00
1.89
1.00
9.71
114
115
157
1820
1620
9160
23
8
780
1860
6400
22
43
57
5050
1770
36
26
4180
6110
603
1590
885
2010
4450
2650
509
310
391
375
1030
123
824
209
793
332
62
68
690
877
818
1250
1420
744
1670
5110
896
471
1330
1180
3970
232
1080
492
3550
2100
218
258
3290
3650
DIN 5 dissolved inorganic nitrogen.
DIP 5 dissolved inorganic phosphorus.
DSi 5 dissolved silicate.
DON 5 dissolved organic nitrogen.
Table 3.
and 2007.
Sta.
Concentrations of Ra isotopes, nutrients, and photosynthetic pigments in surface seawaters off Tongyeong in 2006
Temp.
(uC) Salinity
223Ra
224Ra
Bq
DIN*
m23
DIP{
mmol
DSi{
DON1
Peridinin
L21
Fucoxanthin
ng
Chl a
L21
21–24 Aug 2006
1
26.4
2
26.0
3
27.1
4
27.2
5
27.2
6
26.7
7
28.1
8
28.2
9
27.5
10
28.5
11
28.0
31.7
31.6
31.6
31.4
31.4
31.5
31.4
31.5
31.7
31.4
31.3
—
0.0960.01
0.0660.01
0.1760.03
0.1060.01
0.1060.01
0.0660.01
0.0360.01
0.0860.02
0.1060.02
0.0360.01
—
1.4060.03
0.9460.04
1.5860.06
1.3860.04
0.8960.03
0.9260.03
0.5560.03
0.9660.05
1.1660.05
0.7460.03
2.97
3.23
3.37
2.60
2.41
2.06
2.97
3.53
3.23
3.17
2.80
0.15
0.24
0.03
0.09
0.04
0.10
0.03
0.04
0.10
0.13
0.24
9.54
7.80
7.10
8.27
6.95
7.94
8.86
7.78
4.62
6.61
8.55
—
—
5.08
2.99
4.56
4.91
3.51
3.02
2.98
1.75
4.39
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
949
629
163
709
675
745
823
556
553
607
533
27 Aug 2007
A1
26.2
A2
30.4
A3
24.5
A4
26.7
A5
25.5
33.0
31.9
29.9
33.1
32.6
0.1860.02
0.3760.02
0.1460.02
0.1760.02
0.1360.02
1.3060.05
2.8460.06
0.8960.05
1.5560.05
0.9460.04
8.07
2.69
6.70
3.05
4.17
0.34
0.33
0.45
0.17
0.20
1.20
1.14
3.09
1.82
2.05
2.83
6.95
2.29
4.68
3.47
132
52
1390
2060
2320
783
462
250
408
779
1230
1280
2690
3140
3250
*
{
{
1
DIN 5 dissolved inorganic nitrogen.
DIP 5 dissolved inorganic phosphorus.
DSi 5 dissolved silicate.
DON 5 dissolved organic nitrogen.
Groundwater-borne nutrients traced by Ra
Table 4.
Concentrations of Ra isotopes and nutrients in groundwater around Yeoja Bay in 2007.
223Ra
Date
Sta.
Temp.
(uC)
04 Jul
06 Jul
G7
G1
G2
G3
G5
G2
G4
G7
G5
G6
G7
G2
G5
G6
G7
G8
G9
17.6
18.3
20.6
22.7
17.4
26.5
19.0
24.2
17.8
29.4
23.9
30.4
19.7
27.6
18.7
16.4
28.4
05 Aug
19 Aug
22 Aug
5
Salinity
6.3
1.5
3.3
22.1
26.2
25.2
7.0
25.5
23.5
26.5
6.3
19.8
29.9
28.8
6.5
0.8
1.7
224Ra
DIN*
DSi{
mmol L21
Bq m23
6.060.2
0.160.0
0.460.1
16.960.7
1.960.2
17.760.5
10.660.5
5.360.3
2.260.2
15.260.5
5.760.2
11.160.8
2.160.2
7.960.5
4.160.3
0.560.1
0.560.0
DIP{
8061
260
1360
17962
3561
24063
16363
6761
6762
30565
9762
32069
7362
20366
6462
1361
1360
666
705
2140
767
436
480
507
426
426
541
411
440
438
496
407
968
1420
5.3
6.1
10.1
11.1
10.1
12.1
12.0
12.1
10.9
14.6
11.0
12.9
14.5
14.6
13.3
15.0
33.4
393
137
133
129
277
50
85
305
87
192
285
52
190
161
295
269
165
* DIN 5 dissolved inorganic nitrogen.
{ DIP 5 dissolved inorganic phosphorus.
{ DSi 5 dissolved silicate.
223Ra
and 1.05 6 0.32 Bq m23 for
same area.
224Ra)
to season. Because red tides generally occur in lower
salinity waters that cannot be accounted for by these
stream-water inputs, YRDW is suggested to be the source
of the nutrients that fuel red tides in the study region (Yang
et al. 2000). However, Hwang et al. (2005a) suggested that
the submarine input of brackish groundwater is ,2.6 3
107 m3 d21 in Yeoja Bay, which is about two orders of
magnitude higher than the stream flow, which becomes the
main source of Ra isotopes and nutrients in Yeoja Bay
in 2006 in the
Discussion
Sources of nutrients in red-tide areas—The amount of
freshwater entering into Yeoja Bay is ,1.6 3 105 m3 d21,
from the Beolgyo stream (to the west) and the Isa stream
(to the east), but that amount varies significantly according
Table 5. Concentrations of Ra isotopes and nutrients in surface seawater near Yeoja Island,
located in the center of Yeoja Bay in 2007.
223Ra
Date
05 Jul
06 Aug
18 Aug
21 Aug
24 Aug
Time
(h)
Temp.
(uC)
Salinity
11:05
12:05
13:05
14:35
15:35
16:35
11:28
12:28
14:28
11:33
13:03
15:03
13:06
14:23
12:07
15:07
24.7
24.0
24.7
24.2
24.5
24.3
26.4
27.4
26.7
29.1
30.2
29.1
29.3
30.4
31.1
30.3
28.4
29.4
28.7
29.3
29.2
29.4
31.7
31.5
32.0
26.3
24.7
26.5
26.2
26.5
26.0
27.6
* DIN 5 dissolved inorganic nitrogen.
{ DIP 5 dissolved inorganic phosphorus.
{ DSi 5 dissolved silicate.
224Ra
DIN*
6.7460.09
5.4460.09
6.8360.14
8.4660.09
8.1460.14
7.3560.14
8.6760.09
8.1560.14
8.9060.10
6.9360.08
8.1360.14
8.0060.09
9.5560.19
8.0960.07
6.0560.14
6.6960.19
DSi{
mmol L21
Bq m23
0.6060.03
0.6960.04
0.4360.03
0.7260.03
0.7360.05
0.5360.04
0.6560.03
0.7760.06
0.8260.04
0.5860.03
0.7160.05
0.7560.04
0.8660.07
0.5660.02
0.6860.06
0.7260.07
DIP{
17.0
13.5
11.8
11.1
7.2
11.9
7.2
9.0
11.4
5.7
2.0
1.3
3.5
4.3
4.8
8.5
0.29
0.32
0.33
0.30
0.55
0.24
0.73
0.87
1.05
0.13
0.10
0.10
0.14
0.07
0.03
0.12
30.2
27.1
29.9
27.7
26.2
28.2
29.8
31.2
35.3
12.4
16.8
11.1
11.4
8.7
25.0
22.6
6
Lee et al.
Fig. 2. (A) Map showing sampling stations for open-ocean
waters, including the Yangtze River Diluted Water (YRDW), and
(B) a diagram of 224Ra vs. 223Ra activity in surface seawaters.
Most of the waters (A) observed in the open ocean were
influenced by Yangtze River water (salinity between 30 and 32).
Most of the Ra data (B) were obtained in seawater off Yeoja Bay,
and the filled symbols denote the centers of the red-tide patches.
The upper triangles were from the inner Yeoja Bay. The activities
of 224Ra and 223Ra in YRDW are from Hwang et al. (2003). The
data for 2002 and 2003 are from Lee and Kim (2007).
(Table 1). In this regard, Lee and Kim (2007) showed that
the main source of nutrients that occurred in the offshore
red-tide region in 2002 and 2003 was coastal groundwater,
based on a Ra tracer (Table 1). The activities of Ra
isotopes in the red-tide region in 2007 fell into the mixing
line between Yeoja Bay waters in the northern part of the
red-tide region and open-ocean waters, and these activities
were orders of magnitude higher than those in the lowsalinity YRDW (Hwang et al. 2003; Fig. 2). These results in
2007 are consistent with the previous conclusion (Lee and
Kim 2007) that the excess Ra isotopes (223Ra and 224Ra),
together with nutrients, that occur in the offshore red-tide
region, originate from coastal groundwater (mainly
through Yeoja Bay).
Environmental conditions for red-tide outbreaks—We
used 224Ra as a tracer for offshore nutrients because it is
more sensitive than 223Ra or 226Ra, and the half-life of
224Ra is appropriate for the time scale of water-mixing in
this region. In the study region, the variation in 224Ra
activity was independent of salinity in 2006 and 2007, with
similar salinity (,32) for all stations, although the activity
of 224Ra was inversely correlated to salinity (28–31) in 2002
and 2003 (Fig. 3A). This finding indicates that 224Ra
originated mainly from saline groundwater (i.e., mostly
recirculating seawater) in 2006 and 2007, while it came
mainly from low-salinity groundwater in 2002 and 2003.
This interpretation is based on the assumption that the
inputs of 224Ra from bottom sediments (diffusion) and
surface runoffs are relatively much smaller than those from
groundwater, as suggested in studies conducted in 2003
(Hwang et al. 2005a). Because the intensity of red tides was
largest in 2002 and 2007, the outbreak of red tides was not
directly linked to the salinity of brackish groundwater.
Although there were good correlations between DSi and
224Ra in red-tide areas in 2002 and 2003, the concentrations
of DSi were relatively much lower in 2006 and 2007 (Fig. 3B).
It appears that low-salinity source waters are more DSienriched. The level of DSi was not directly linked to the
outbreak of red tides in this region (Lee and Kim 2007). In
the red-tide region, the concentrations of either DIN or DIP
were almost completely depleted in those four study years
(Fig. 3C,D). Thus, the outbreak of red tides seems to be
associated with depletion of either DIN or DIP, which is
favorable for blooming of dinoflagellates in competition with
diatoms (Kim et al. 2006; Lee and Kim 2007). Similarly, Lee
and Kim (2007) showed that red tides do not occur inside
Yeoja Bay from a transect observation from inside Yeoja Bay
to the offshore red-tide areas because higher concentrations
of DIN and DIP inside Yeoja Bay are more favorable for
diatoms in competition with dinoflagellates.
Because the main sources for DIN, DSi, and 224Ra are
groundwater (Hwang et al. 2005a) and they were wellcorrelated with one another in 2002 and 2003 in this region
(Lee and Kim 2007), such depletion of DIN or DIP relative
to conserved 224Ra should be caused by efficient utilization of
inorganic nutrients by biota. Although inorganic nutrients
are depleted, a supply of energy to fuel red-tide biomass is
necessary. Recent studies reported that C. polykrikoides,
which is one of the major red-tide species in this region, can
utilize DON and DOP (Kim et al. 2007; Kudela et al. 2008)
and even can take up small-size cryptophytes (, 11 mm
equivalent spherical diameter) by engulfing the prey through
the sulcus (Jeong et al. 2004). The concentrations of DON
were two to six times higher than those of DIN in the study
region in 2006 and 2007 (Tables 2, 3). Thus, as shown by
2002 and 2003 results (Lee and Kim 2007), the outbreak of
red tides is associated with the enhanced organic nutrients
under depleted DIN or DIP conditions. Because the direct
contribution of DON through SGD was negligible on the
basis of DON : DIN ratios in groundwater samples, DIN
introduced by SGD in Yeoja Bay might have been efficiently
transformed into DON before or after the bay water moved
to the offshore red-tide areas where direct inputs of DIN are
limited in summer.
Groundwater-borne nutrients traced by Ra
7
Fig. 3. Plots of 224Ra activity vs. (A) salinity, (B) DSi, (C) DIN, and (D) DIP concentrations
in 2002, 2003, 2006, and 2007 in surface seawater outside Yeoja Bay. The filled symbols denote
the centers of the red-tide patches. The data for 2002 and 2003 are from Lee and Kim (2007).
Intensity of red tides and groundwater-origin nutrients—
In previous sections, we showed the consistency of our
results in 2006 and 2007 with those in 2002 and 2003, in
terms of nutrient sources and environmental conditions of
red-tide outbreaks in the red-tide region. In this section, we
offer new information that daily or yearly changes in
intensity of red tides are associated with magnitude of
groundwater-borne nutrient flux into the red-tide region.
This is based on assumptions that 224Ra (1) is chemically
and biologically conservative in the red-tide region, (2)
originates mainly from groundwater (Hwang et al. 2005a),
and (3) is correlated to the nutrients in the source region
(Lee and Kim 2007).
The composition of chemical species, such as Ra and
nutrients, was similar in both red-tide patch and nonpatch
areas in 2007 (Table 2). In order to estimate physical
aggregation factors of red-tide patches, we calculated the
ratios of Chl a to 224Ra for patch and nonpatch stations
(Fig. 4). The ratios were ,783–1623 and 95–711 for patch
and nonpatch stations, respectively. If we assume that
biomass in water correlates to the activity of 224Ra in the
water (nutrient supply), red-tide biomass was enhanced by
a factor of 3–9 over that in a nonpatch area by aggregation.
Although there is a large uncertainty in this estimate, it is
nonetheless meaningful because it reflects the first estimation of magnitude of an aggregation effect by physical
factors (i.e., currents, waves, and fronts) that occur in redtide areas (Jeong et al. 2000; Park et al. 2005).
In 2007, the first red tide occurred on 31 July in the
coastal area off Kuemhodo. The occurrence of dinoflagellate red tides peaked around 11 August, with a cell density
of 1250–8970 cells mL21 (C. polykrikoides; Bae et al. 2008).
Subsequently, the cell density decreased gradually below
1000 cells mL21 until 11 September. Similarly, peridinin, an
index pigment of dinoflagellates, was ,115 ng L21 on 17
August 2007; it then decreased below 50 ng L21 at
nonpatch stations (Sta. 1 and 2) on 25 August (Table 2).
Both Chl a and 224Ra activity decreased gradually after the
red-tide peak on 11 August 2007 at both red-tide patch and
nonpatch stations (Fig. 5). This trend indicates that the
decrease of groundwater-borne nutrients (derived on the
basis of 224Ra activities) causes the decline of red-tide
intensity.
The age of groundwater-borne nutrients occurring in
offshore red-tide areas was calculated using a 224Ra : 223Ra
ratio model suggested by Moore (2000), on the basis of a
8
Lee et al.
Fig. 4. Plots of chlorophyll a concentrations vs. 224Ra
activities in surface seawater in the red-tide region in 2007. The
filled symbols denote the centers of the red-tide patches.
change in groundwater-borne Ra ratios by decay from an
average Ra activity in groundwater samples (Table 4). Age
was ,6.0 6 1.6 d (average) in offshore red-tide areas in
2007, which is similar to the mean residence time (,7 d) of
Yeoja bay water (Hwang et al. 2005a). Age increased from
17 August (4.5 6 0.9 d) to 25 August (6.7 6 0.5 d) over the
time-series sampling periods together with decreasing 224Ra
activity and pigments, thereby indicating that a decrease of
new Ra (and nutrient) supply causes a decrease of the redtide intensity (Figs. 4, 5).
Such a control of groundwater-borne nutrients on the
intensity of red tides is also apparent for different years
(Fig. 6). In order to compare the intensity of the red tides
for each year, the maximum daily cell counts (C.
polykrikoides) in patch areas were averaged for a period
from 01 August to 31 August in the study region. Larger
intensity of red tides (average of 1 month) in 2002 and 2007
is well-matched with the enhanced level of 224Ra activity,
compared with 2003 and 2006. Outbreak of red tides was
not observed in seawater off Tongyeong in 2006 when
relatively much lower 224Ra activity was observed, compared with 2007.
Therefore, both daily and yearly variations in red-tide
intensity on a regional scale clearly suggest that the
intensity of red tides is controlled by the magnitude of
groundwater-borne nutrient introduction into the offshore
red-tide region. Our conclusion based on a Ra tracer is
different from suggestions of some previous researchers
(Yang et al. 2000; Lee and Kang 2003) that offshore
dinoflagellate red tides were not linked to nutrient supply
because they observed only inorganic nutrients.
Over the same study period in 2007, the activities of
224Ra and 223Ra were almost constant at the Yeoja Bay
monitoring site (Fig. 5C), which is the source region of
Fig. 5. The temporal variation in 224Ra activities and
chlorophyll a concentrations in (A) red-tide patch areas (one
station on 17 and 20 Aug; two stations on 23 and 25 Aug), (B)
non-patch areas (Sta. 1 and 2), and (C) temporal variation in
224Ra and 223Ra activities in surface seawater near Yeoja island
located at the center of inner Yeoja Bay.
groundwater-borne nutrients that discharged into the
offshore red-tide region (Hwang et al. 2005a). Thus, we
suggest that the magnitude of groundwater-borne nutrient
export into red-tide areas is associated with local conditions
of inner-bay water expansion to offshore areas by physical
processes (i.e., fronts and currents) rather than with any
temporal change in magnitude of SGD.
In summary, SGD introduces a large amount of
inorganic nutrients to Yeoja Bay (enough for fueling red
tides in summer), and the inorganic nutrients are transformed almost entirely to organic forms when or after
Yeoja Bay water arrives at offshore red-tide areas because
direct inorganic nutrient sources are limited in red-tide
areas in summer. Red tide initiates when DIN or DIP is
Groundwater-borne nutrients traced by Ra
9
Fig. 6. The size of patch areas integrated for 1 month between 01 and 31 August in 2002, 2003, 2006, and 2007 in the southern sea of
Korea. Maximum daily cell counts (C. polykrikoides) in patch areas were averaged for a period from 01 August to 31 August in the study
region. The quadrangles represent the sampling sites. The activities of 224Ra measured from the observational studies are shown for
each year.
almost completely depleted, while dissolved organic nutrients are increased, favorable for the growth of dinoflagellates in competition with diatoms. The intensity and
duration of red tides appear to be controlled mainly by
physical transport of bay water into the offshore red-tide
areas. Thus, further physical–chemical–biological cooperative studies are necessary to predict conditions of harmful
algal bloom dynamics in the future. In order to manage red
tides that occur in offshore waters, we should understand
daily and seasonal expansion of shallow coastal water to
offshore areas, and we should act to reduce the pollution
from nitrogen and phosphorus in coastal groundwater in
the future.
Acknowledgments
We thank all Environmental & Marine Biogeochemistry
Laboratory members who supported field sampling and lab
analyses. This research was supported by the Korea Science &
Engineering Foundation through the Basic Research Program
(KOSEF, R01-2006-000-10646-0) and National Research Laboratory (R0A-2008-000-20055-0).
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Associate editor: Samantha B. Joye
Received: 06 August 2008
Accepted: 11 May 2009
Amended: 03 July 2009