PUBLICATIONSJournal of Geophysical Research: Biogeosciences
RESEARCH ARTICLE
10.1002/2017JG004088
Key Points:• Promotion effect of Asian dust on
phytoplankton growth is conﬁrmed
by incubation experiments in theSouth China Sea• Comprehensive analysis ofphytoplankton growth reveals
potential utilization of dissolved
organic phosphorus• Oligotrophic and ultraoligotrophic
conditions were identiﬁed, leading todifferent phytoplankton responses toexternal inputs

Promotion Effect of Asian Dust on Phytoplankton Growthand Potential Dissolved Organic Phosphorus
Utilization in the South China Sea
Qiang Chu1,2, Ying Liu1,3, Jie Shi1,4 , Chao Zhang1, Xiang Gong5, Xiaohong Yao1
Xinyu Guo1,2 , and Huiwang Gao1,4,

1
Key Laboratory of Marine Environment and Ecology, Ocean University of China, Ministry of Education of China, Qingdao,
China, 2Center for Marine Environmental Studies, Ehime University, Matsuyama, Japan, 3Now at College of Chemistry,
Chemical & Environmental Engineering, Weifang University, Weifang, China, 4Laboratory for Marine Ecology andEnvironmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China, 5School ofMathematics and Physics, Qingdao University of Science and Technology, Qingdao, China

Abstract Dust deposition is an important nutrient source to the South China Sea (SCS), but few in situ
Supporting Information:• Supporting Information S1• Data Set S1• Data Set S2Correspondence to:
H. Gao,hwgao@ouc.edu.cn

Citation:Chu, Q., Liu, Y., Shi, J., Zhang, C., Gong, X.,
Yao, X., et al. (2018). Promotion effect ofAsian dust on phytoplankton growthand potential dissolved organic
phosphorus utilization in the South
China Sea. Journal of GeophysicalResearch: Biogeosciences, 123. https://doi.org/10.1002/2017JG004088
Received 1 AUG 2017
Accepted 7 FEB 2018
Accepted article online 14 FEB 2018

experiments were conducted on phytoplankton response to the deposition. We conducted onboard
incubation experiments at three stations near Luzon Strait in the SCS, with addition of multiple dissolved
inorganic nutrients, Asian dust, and rainwater. From our results, nitrogen and phosphorus were bothurgently needed for phytoplankton growth in the SCS, indicated by the evident Chl a response to theaddition of nitrogen and phosphorus together. Almost no evident response was observed by adding
phosphorus or iron alone to incubation waters, although a delayed response of Chl a in massconcentration was observed by adding nitrogen alone. The latter implied a possible utilization of dissolved
organic phosphorus because of insufﬁcient dissolved inorganic phosphorus in incubation waters. Under
such nutrient condition, Asian dust showed an apparent promotion effect on phytoplankton growth byproviding sufﬁcient amounts of nitrogen but low phosphorus. Meanwhile, it was found that large sized(> 5 μm) phytoplankton community showed different responses to dust addition at different stations. At
stations A3 and A6, Chaetoceros spp. became the dominant species during the bloom period, while atstation WG2, Nitzschia spp. became dominant. In combination with different initial nutrients and Chl alevels at the three stations, the different phytoplankton community evolution implied the response
difference to external inputs between oligotrophic (stations A3 and A6) and ultraoligotrophic (station
WG2) conditions in the SCS.

1. Introduction
Atmospheric deposition is important to the ocean by providing large amount of bioavailable elements,
among which dust events play a vital role (Duce et al., 2008; Jickells et al., 2005). Asian dust is reported to
be one of the largest source of dust and can be transported more than thousands of kilometers eastward overthe East Asian continent and the Paciﬁc Ocean in spring (Shao et al., 2011; Zhao et al., 2003). During the transport of Asian dust, it can deposit and thereby supply bioavailable nutrients (N, P, Si, etc.) and trace metals (Fe,Mn, etc.) to the ocean, which is considered to have a signiﬁcant inﬂuence on marine ecosystems (Tan et al.,2011; Wang et al., 2012). The fertilization effect of dust has been reported in oligotrophic Mediterranean Sea
and Atlantic Ocean (Mills et al., 2004; Ridame et al., 2014), as well as in western North Paciﬁc Ocean (Yuan &Zhang, 2006) and coastal China seas (Tan et al., 2011), for example, in the Yellow Sea (Shi et al., 2012) and theSouth China Sea (SCS) (Wang et al., 2012).

©2018. American Geophysical Union.
All Rights Reserved.

CHU ET AL.

In marine ecosystems, changes in nutrient availability occur on different temporal and spatial scales, affecting
elemental stoichiometry, primary production, and limiting conditions (Arrigo, 2005; Eppley & Peterson, 1979).
Nitrogen is the limiting nutrient for phytoplankton growth in the low-latitude open ocean (Moore et al., 2013;
Vitousek & Howarth, 1991). Iron is considered to limit phytoplankton growth in high-nutrient low-chlorophyll
regions (Boyd et al., 2000; Tsuda et al., 2003). Meanwhile, iron can also be the limiting nutrient in oligotrophic
regions due to its effect on nitrogen ﬁxation (Wu et al., 2003). Phosphorus is considered to be the limiting
nutrient in the Mediterranean Sea (Thingstad et al., 2005) and is treated as a secondary limiting nutrient in
the open ocean (Moore et al., 2013). In addition, dissolved organic phosphorus (DOP) contributes to algae

1Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

growth in low dissolved inorganic phosphorus (DIP) concentration
conditions (Lin et al., 2012; Lomas et al., 2010).
Through satellite and ﬁeld observations, enhancement of primary
production by atmospheric deposition has been revealed (Shi et al.,2012; Tan et al., 2011). Nutrient enrichment bioassays, especially in situ
incubation experiments, are widely used to directly evaluate the limiting
condition and oceanic responses to dust deposition in oligotrophic oceans(Davey et al., 2008; Giovagnetti et al., 2013; Moore et al., 2008). Some
onboard incubation experiments have also been carried out in the marginal seas of China, including both shelf and basin regions, to investigate
the planktonic response to nutrients and dust addition (Guo et al., 2012;
Liu et al., 2013). To integrate analysis of nutrient and plankton dynamics
in mesocosm incubations, models were developed in some studies for speciﬁc experiments (Thingstad et al., 2007; Van den Meersche et al., 2004). A
combination of in situ experiments and models can better explain theseprocesses in various marine ecosystems.
The SCS is one of the largest marginal seas in the world and is located in
the western North Paciﬁc Ocean (Chen et al., 2004). It is an oligotrophic
region with deep euphotic zone (Wong et al., 2007). The nitracline depth(depth where dissolved inorganic nitrogen (DIN) equals 0.1 μmol/L)(Herbland et al., 1985) varies from 20 m in winter to 80 m in summer
Figure 1. Sampling stations in the South China Sea.
(Chen, 2005). Bordering on East Asia continent, the SCS, especially thenorthern part, is readily affected by Asian dust deposition mixed withanthropogenic aerosols (Wang et al., 2011) during the monsoon season (Zhang et al., 1997). The depositionof Asian dust and anthropogenic aerosols can increase biomass and primary production, promote the phytoplankton blooms, and change the phytoplankton community structure (Guo et al., 2012; Wang et al., 2012).
However, limiting conditions and the marine ecosystem response to atmospheric deposition, especially theentire processes including blooming and extinction period, remain poorly understood due to the lack of insitu studies in the SCS. In our research, we conducted onboard incubation experiments to assess the responseof phytoplankton communities to nutrient, dust, and rainwater deposition in the SCS. Also, a biogeochemical
box model was used to improve understanding of biological processes during incubation experiments. This
study aims to (1) assess the nutrient-limiting conditions for the phytoplankton growth in the SCS and (2) investigate the effect of Asian dust on the biogeochemistry and community structure in the incubation system.

2. Materials and Methods
Onboard incubation experiments were conducted during the cruise of R/V Dongfanghong 2 from 21 March to
2 May 2013 in the SCS. Sampling and experiments were conducted at station A3 (120.50°E, 20.50°N) startingon 27 March, at station A6 (120.50°E, 19.00°N) starting on 12 April, and at station WG2 (119.64°E, 18.00°N)
starting on 23 April (Figure 1). All three sampling stations were located near the Luzon Strait. Station WG2
is closer to the basin of the SCS (Figure 1) and is the deepest among the three stations (Table 1).
2.1. Experimental Design
The incubation experiments with durations of 13, 11, and 10 days, including the seawater sampling day (day0), were conducted at station A3, station A6, and station WG2, respectively. Surface seawater (2–5 m in depth)
was collected with Niskin bottles mounted on a Seabird CTD (Conductivity, Temperature, Depth, SBE 911
plus, USA). The collected water was distributed into 16 acid-cleaned 20 L Nalgene polycarbonate incubation
bottles after ﬁltering through 200 μm nylon mesh to exclude mesozooplankton. We avoided contacting trace
metals by using acid-cleaned plastic or polymeric material equipment in the experiment setup and sampling
processes, despite the experimental operation was not in rigorous trace metal clean environment.
The bottles were divided into eight groups (two replicates) as described in Table 2: control group, N group, P
group, Fe group, N + P group, N + P + Fe group, dust group, and rainwater group. All the bottles were placedin transparent plastic vessels on the deck and bathed with running seawater pumped from sea surface to

CHU ET AL.

2

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Table 1
Nutrient Concentrations at Each Station on Day 0 of the Incubation Experiments


StationIncubation
start
date

NO3

Depth
(m)

A3
A6
WG2

2,700
3,161
3,963

27 Mar
12 Apr23 Apr

0.31
0.55
0.05

NO2



3

PO4

SiO3

2

(μmol/L)
0.04
0.04
0.05

0.08
0.02
0.01

2.21
2.67
2.31





Chl a

[NO3 + NO2 ]/PO4(μg/L)

—

0.14
0.14
0.04

4.4
29.5
10.0

3

maintain in situ temperature throughout the incubation (Liu et al., 2013). All bottles were gently stirred threetimes a day to avoid biogenic accumulation.
For dust group, 1/16 of a dust-collected ﬁlter (the dust was assumed to be uniformly collected on the ﬁlter)
was placed in 20 mL Mill-Q water and extracted with ultrasonication for 1 h at 0°C (Guo et al., 2012; Hsu et al.,2010). Then, the ﬁlters and turbid solution were added to each of two incubation bottles. With above procedures, the dust added to each bottle was about 1.09 mg/L. The annual dust deposition in the SCS is estimatedto be in a range of 2.5–52 g/m2 (Gao et al., 1997; Wang et al., 2012). Assuming deposited dust was distributed
evenly in the mixed layer whose depth ranges from 27 to 57 m (shallow in summer and deep in winter) (Chen& Chen, 2006), the annual dust input to surface seawater becomes approximately 0.04–1.9 mg/L. The addedconcentration of 1.09 mg/L in the dust group was at the middle of the annual dust deposition range.
For the rainwater group, 8 mL of rainwater was added to each of two bottles. The amount of added rainwater
was under an assumption of a heavy rain event (20 mm) into a 50 m mixed layer depth.
For the elemental addition groups (N, P, and Fe added individually and in combination), the levels wereselected to evaluate the limiting condition in the SCS and to identify the key element in dust affecting themarine ecosystem. The nutrients were added in concentrations based on previous incubation experimentsin the SCS (Guo et al., 2012) and the Yellow Sea (Liu et al., 2013).
2.2. Dust and Rainwater Collection and Chemical Analysis
Asian dust samples were collected during the dust storm period of 9–10 March 2013. Samples were collectedon Whatman 41 cellulose ﬁlters using a high volume sampler (KC-1000, Qingdao Laoshan Elec. Inc., China),
placed at the Laoshan campus of Ocean University of China, Qingdao (36.10°N, 120.27°E). Our dust collection
palace was in northern China, which was located in the pathways of eastward transported Asian dust, before
branching southward to the SCS (Tan et al., 2012; Wang et al., 2011). During the 24 h sampling period(1.05 m3/min), about 0.348 g of total suspended particles was collected. The ﬁlter was stored at 20°C until
chemical analysis and use in incubation experiments.
To measure the dissolvable materials that leached from dust samples, a piece of the ﬁlter was placed in 20 mL
Mill-Q water and extracted with ultrasonication for 1 h at 0°C (Guo et al., 2012; Hsu et al., 2010). The solution
was ﬁltered with acid-cleaned acetate cellulose ﬁlters (0.45 μm poresize) and rinsed three times with Mill-Q water. Dissolved inorganic
Table 2nutrients were analyzed by Nutrient AutoAnalyzer (SEAL Analytica,
Treatment in Different Incubation Groups
AutoAnalyzer 3). For dissolved trace metals, the ﬁltered solution wasGroup
Treatment
acidiﬁed and assayed by inductively coupled plasma atomic emission
Control
spectrometry (Hsu et al., 2010; Shi et al., 2012).
N group
P group
Fe group
N + P group
N + P + Fe group
Dust group
Rainwater group

2 μmol/L NaNO3
0.2 μmol/L NaH2PO4
2 nmol/L FeSO4
2 μmol/L NaNO3 + 0.2 μmol/L NaH2PO4
2 μmol/L NaNO3 + 0.2 μmol/L
NaH2PO4 + 2 nmol/L FeSO4
a
1.09 mg/L dustb
0.4 mL/L rainwatera
Nutrients added by dust: N, 0.57 μmol/L; P, 7.27 nmol/L; Fe, 8.67 nmol/L.
b

Nutrients added by rainwater: N, 0.045 μmol/L; P, 0.36 nmol/L; Fe,
0.16 nmol/L.

CHU ET AL.

Rainwater (pH 4.95) was collected on 24 March 2013 during the cruisein the SCS before the incubation experiments. Acid-cleaned polyethylene bottles were placed on the upper deck of the ship for rainwatercollection. The collected rainwater was stored at 20°C until chemical
analysis and incubation experiments. The rainwater samples foranalysis were thawed and then ﬁltered and analyzed in the same
way as the dust sample. In preparation for trace metals analysis,
acidiﬁcation was conducted by adding 5% ultrapure HNO3
(Al-Momani, 2003).

3

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Table 3
Dissolved Nutrients and Trace Metals in Dust and Rainwater Samples Collected Before Incubation Experiments
Nutrients (μmol/g)
Dust sample

Rainwater sample


NO3


NO2

166.70

5.51



NO3
48.16

+

3
PO4

NH4
355.90
6.66
Nutrients (μmol/L)

+
3
NO2
NH4
PO4
0.24
63.95
0.91

Trace metals (μg/g)
2
SiO3

1.57
2

SiO3
1.03

Pb
32.25

Cr
29.11

Mn
3.15

Fe
445.40

Pb
18.74

Cr
3.34

Mn
0.37

Fe
22.70

Co
Ni
Cu
2.65
31.67
100.20Trace metals (μg/L)
Co
Ni
Cu
0.24
2.24
20.12

Zn
281.90

As
21.24

Cd
0.98

Zn
97.95

As
1.03

Cd
0.13

2.3. Sampling in the Incubation Experiments and Analysis
2.3.1. Chl a and Nutrients
Duplicate 300 mL (for Chl a concentration) and 150 mL (for nutrient concentration) samples were collectedfrom each incubation bottle at the same time in the morning during the incubation period. The subsamples
for Chl a measurements were ﬁltered through acid-cleaned Whatman GF/F glass ﬁber ﬁlters (0.7 μm poresize). Chl a ﬁlters were extracted with 90% acetone at 20°C in the dark for ~24 h (Strickland & Parsons,1972). Then the Chl a concentration was measured using a Turner Design Fluorometer (Turner Designs,
Trilogy Laboratory Fluorometer, USA) (Guo et al., 2012).
The subsamples for dissolved inorganic nutrient concentration were ﬁltered through acid-cleaned acetate
cellulose ﬁlters (0.45 μm pore size). Then the ﬁltrate was stored in acid-cleaned polyethylene bottles at
20°C until analysis in the laboratory. Subsamples for dissolved inorganic nutrients were analyzed by the
Nutrient AutoAnalyzer (SEAL Analytica, AutoAnalyzer 3). The limit of detection for NH4+, NO3, NO2,SiO32, and PO43 were 0.04, 0.02, 0.003, 0.005, and 0.01 μmol/L, respectively.
2.3.2. Phytoplankton Community Identiﬁcation
A 300 mL water sample for phytoplankton community identiﬁcation was collected in the morning at thesame time as the Chl a and dissolved inorganic nutrient collection. The sampling for phytoplankton community identiﬁcation was on the following schedule: days 0, 4, 8, and 12 at station A3; days 0, 4, and 8 at station
A6; and days 0, 4, 7, and 9 at station WG2. Samples were immediately ﬁxed with acidic Lugol’s iodine (2% ﬁnal
concentration) and stored in the dark (Stibor et al., 2004). In preparation for analysis, the samples wereconcentrated to 10–15 mL by settling for 48 h in glass cylinders and ﬁnally examined by an inverted microscope (Nikon ECLIPSE TE2000-U) for identiﬁcation of phytoplankton >5 μm in size. We took one parallel
sample for the presentation of phytoplankton community, with the other parallel sample as an alternativein case the sample is broken.

3. Results
For initial seawater, slightly high DIN (0.35 μmol/L ≤ NO3 + NO2 ≤ 0.59 μmol/L) and DIP (0.02 μmol/L ≤PO43 ≤ 0.08 μmol/L) concentrations were observed at stations A3 and A6, compared to low concentrations(NO3 + NO2 = 0.10 μmol/L, PO43 = 0.01 μmol/L) at station WG2 (Table 1). Other studies also reported asimilar variation range of DIN (0.01–0.31 μmol/L) and DIP (0.01–0.09 μmol/L) in the spring SCS, with the ratioof N/P lower than the Redﬁeld ratio of 16 (Chen et al., 2004; Wu et al., 2003). For the Chl a, which was treatedas the proxy for phytoplankton biomass, we observed a variation range from 0.04 μg/L (station WG2) to
0.14 μg/L (stations A3 and A6) in our experiment (Table 1), which was comparable with the results in anotherstudy (Chen, 2005).
The dissolved inorganic nutrients and trace metals leached from the dust and rainwater are shown in Table 3.
The concentration of total dissolved inorganic nitrogen (528.11 μmol N/g, including NO3, NO2, and NH4+)
was relatively higher than other nutrients in both the dust and rainwater. The high N/P ratio in dust (79:1) andrainwater (123:1) implied that they supplied more nitrogen than phosphorus for phytoplankton.
3.1. Station A3
3.1.1. Chl a and Nutrients
Chl a for the N + P and N + P + Fe groups at station A3 was statistically signiﬁcantly higher than that of thecontrol group (PN + P < 0.05, PN + P + Fe < 0.05) with maximum values of 1.87 μg/L and 3.22 μg/L, respectively,that were 3.1-fold and 5.4-fold of the maximum Chl a in the control group (0.60 μg/L) (Figure 2a). The
maximum value in the N group (1.60 μg/L) was 2.7-fold of the control group (PN < 0.01), but the individual
CHU ET AL.

4

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Figure 2. Measured Chl a concentration in nutrient addition groups (a) and dust and rainwater addition groups (b) at station A3; (c) and (d) show the same respective
additions at station A6; and (e) and (f) show the same respective additions at station WG2.

addition of P or Fe did not produce an increase in Chl a. The maximum value in the N group occurred on day
9, which is later than the peak in the N + P group on day 7 and in the N + P and N + P + Fe groups on day 6.
Both the positive response in the N and N + P groups and the negative response in the P group wereconsistent with previous researches in the SCS (Chen, 2005; Wu et al., 2003). The maximum Chl a in the
dust group (Pdust < 0.05) reached 1.28 μg/L on day 5, which was about 2.1-fold of that in the control group(Figure 2b). The addition of rainwater induced no response in Chl a.
Consistent with the increase in Chl a in nitrogen-related groups, nutrient concentrations in these groups
decreased. DIN decreased to 6%, 11%, and 11% of initial values in the N, N + P, and N + P + Fe groups(Figure 3) at the time of reaching the maximum Chl a. DIP in these groups showed a similar deceasing trend.
In the rainwater group, DIN and DIP provided by rainwater was 12.9% and 0.45% of that in backgroundseawater. Thus, DIN and DIP concentrations were low in the group during the incubation, which were similar
to that in the control group. Nutrients also showed a decreasing pattern in the dust group. Interestingly, in

CHU ET AL.

5

Journal of Geophysical Research: Biogeosciences





3

10.1002/2017JG004088

2

Figure 3. Measured nutrient concentrations in all incubation groups at three sites. (a)–(c) NO3 + NO2 , PO4 , and SiO3
concentrations at station A3;


3
2


3
2
concentrations at station A6; (g)–(i) NO3 + NO2 , PO4 , and SiO3
concentrations at station WG2.
(d)–(f) NO3 + NO2 , PO4 , and SiO3

the N + P group, Chl a did not show a rapid increase in the ﬁrst 4 days despite the fast decrease of nutrients.
This result may reﬂect luxury uptake and storage of DIN and DIP by the algae (Lomas et al., 2010; Vincent,1981). The decease of silicate in groups without an increase in Chl a (e.g., control and rainwater groups)
also conﬁrmed this occurrence. DIP in the N group was low during the incubation. On the contrary, Chl ain the N group showed an obvious increase in extremely low DIP, which indicated supplementation fromother phosphorus sources. The slowly increasing trend of Chl a implied the slow transformation andassimilation of that phosphorus source.
3.1.2. Phytoplankton Community
In this study, 47 genera or species were recorded. Algae species from the same genera were not separately
recoded. In the results, Climacodium spp., Chaetoceros spp., Nitzschia spp., Leptocylindrus spp., andLicmophora spp. were the dominant diatom species.
At station A3, the initial phytoplankton community (total abundance, 4.2 × 104 cells/L) was composed of diatoms, dinoﬂagellates, and cryptomonas with abundance percentages of 80.7%, 10.4%, and 8.9%, respectively(Table 4), and very few Chrysophyta was also recorded. The dominant species was Climacodium spp. with anabundance of 1.7 × 104 cells/L. The community structure showed obvious changes during the incubation. On
day 4, Chaetoceros spp. became the dominant species in all the eight groups, especially in the N + P and
N + P + Fe groups (relative abundance >80%) (Table 4). On day 8, Chaetoceros spp. continued to be the dominant algae in N + P and N + P + Fe groups, while in other groups, the dominant algae transitioned to different
algae like Nitzschia spp., Leptocylindrus spp., or dinoﬂagellates. During the bloom period shown by Chl aconcentration from days 4 to 8 in the N + P and N + P + Fe groups, the community structure showed thecompetitive advantage of Chaetoceros spp. in these groups.
3.2. Station A6
3.2.1. Chl a and Nutrients
The responses of Chl a in all incubation groups at station A6 were almost the same as those in corresponding
groups at station A3 (Figures 2c and 2d). N + P and N + P + Fe groups showed an obvious Chl a increase withpeak values of 3.42 and 4.77 μg/L, respectively, which are higher than those in other groups. Chl a in the
CHU ET AL.

6

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Table 4
Phytoplankton Community During Incubation Experiments at Station A3
Day 0
Group
Control
N
P
N+P
Dust
RainwaterFe
N + P + Fe
a

Day 4
a

Dominant
algae

Abundance(proportion)b

Climacodium spp. 1.7 (40.7%)b4

Unit of algae abundance is 10 cells/L.

Day 8
a

Day 12aaDominant
algae

Abundance(proportion)

Dominant
algae

Abundance(proportion)

Dominant
algae

Abundance(proportion)

Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.

5.0 (44.8%)
12.6 (77.6%)
7.5 (55.1%)
8.5 (95.1%)
8.8 (44.7%)
5.3 (70.3%)
5.0 (53.0%)
33.3 (87.7%)

Nitzschia spp.
Leptocylindrus spp.
Nitzschia spp.
Chaetoceros spp.
—
Dinoﬂagellate
Leptocylindrus spp.
Chaetoceros spp.

3.5 (37.0%)
21.2 (56.4%)
3.4 (38.9%)
28.9 (37.7%)—
4.3 (48.8%)
1.4 (38.1%)
13.4 (42.9%)

Dinoﬂagellate—
Nitzschia spp.
Licmophora spp.
Leptocylindrus spp.
Leptocylindrus spp.
Nitzschia spp.
Chaetoceros spp.

2.9 (36.2%)—
2.4 (35.4%)
55.7 (75.5%)
25.8 (58.2%)
8.4 (55.1%)
2.5 (33.1%)
5.6 (31.6%)

4

Total abundance on day 0 is 4.2 × 10 cells/L.

N + P + Fe group reached its peak 1 day earlier than in the N + P group. The N group showed a slow increaseof Chl a that reached its highest value of 1.47 μg/L on the last day of the incubation. In the dust group, Chl aincreased during the ﬁrst 5 days and reached its peak (1.13 μg/L) even earlier than did the N + P + Fe group.
The control and rainwater groups both showed similar more gradual and much smaller increases in Chl a.
For the nutrient additions, DIN and DIP exhibited obvious decreases in the nitrogen-related groups, especiallyin the N + P and N + P + Fe groups. Differing from station A3, DIN and DIP did not decrease until the Chl abloom period during incubation days 4 to 8 (Figure 3). Silicate decreased in all groups at station A3, which
also supported the luxury uptake of silicate in the incubation system.
3.2.2. Phytoplankton Community
At station A6, the total abundance of phytoplankton was 2.6 × 104 cells/L, which is lower than that at station
A3. The composition of diatoms, dinoﬂagellates, and cryptomonas was 77.7%, 12.6%, and 9.7%, respectively.
Although Nitzschia spp. was the dominant species (Table 5) at the beginning of the incubation, Chaetoceros
spp. became dominant in all groups on days 4 and 8, and its proportion exceeded 50% in most groups. The
consistency of the dominance of Chaetoceros spp. in N + P and N + P + Fe groups on days 4 and 8 at both
stations A3 and A6 showed that Chaetoceros spp. was competitive in nutrient-enriched environments.
These results were consistent with previous studies showing that Chaetoceros spp. and Nitzschia spp. were
dominant diatoms in nutrient-enriched winter waters of the SCS (Chen, 2005). Further, the community succession for dust addition seems to be consistent with N + P and N + P + Fe addition during the bloom period.
3.3. Station WG2
3.3.1. Chl a and Nutrients
Surface seawater was more oligotrophic at station WG2 than at stations A3 and A6 (Table 1). Phytoplankton
showed a positive response in all the groups except for the Fe group (Figures 2e and 2f). The maximum Chl a

Table 5
Phytoplankton Community During Incubation Experiments at Station A6
Day 0

Day 4
a

Group

Dominant algae

Abundance (proportion)

Control
N
P
N+P
Dust
RainwaterFe
N + P + Fe

Nitzschia spp.

2.0 (75.4%)

a

b

4

Unit of algae abundance is 10 cells/L.

CHU ET AL.

b

Day 8

Dominant algaeaAbundance (proportion)

Dominant algae

Abundance (proportion)aChaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.

5.1 (69.8%)
1.1 (58.7%)
0.6 (53.4%)
1.1 (54.9%)
6.0 (54.1%)
2.7 (59.7%)
1.1 (49.9%)
3.3 (74.5%)

Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.
Chaetoceros spp.

4.5 (75.7%)
7.7 (75.9%)
2.7 (57.8%)
47.4 (51.2%)
7.6 (68.5%)
1.2 (51.3%)
6.5 (86.1%)
90.7 (80.7%)

4

Total abundance on day 0 is 2.6 × 10 cells/L.

7

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Table 6
Phytoplankton Community During Incubation Experiments at Station WG2
Day 0
Group
Control
N
P
N+P
Dust
RainwaterFe
N + P + Fea

Dominantalgae
Dinoﬂagellate

Day 4
a

Abundance(proportion)b

0.3 (69.5%)

4

Unit of algae abundance is 10 cells/L.

b

Day 7
a

Dominant
algae

Abundance(proportion)

Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.

2.1 (71.1%)
4.3 (67.4%)
5.8 (57.6%)
105.4 (94.5%)
11.0 (96.4%)
28.9 (97.4%)
4.3 (68.5%)
64.4 (89.9%)

Day 9
a

a

Dominant algae

Abundance(proportion)

Dominant algae

Abundance(proportion)

Nitzschia spp.
Chaetoceros spp.
Nitzschia spp.
Dinoﬂagellate
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.

4.6 (79.3%)
5.8 (72.0%)
17.0 (47.9%)
6.0 (51.0%)
16.4 (97.6%)
9.4 (92.1%)
6.5 (76.8%)
35.6 (87.1%)—
Chaetoceros spp.
Leptocylindrus spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.
Nitzschia spp.

—
27.7 (91.5%)
3.2 (54.2%)
3.4 (41.0%)
30.9 (98.3%)
8.9 (87.1%)
2.6 (53.7%)
12.2 (74.3%)

4

Total abundance on day 0 is 0.37 × 10 cells/L.

concentration in the N + P and N + P + Fe groups was 4.9-fold and 7.9-fold of that in the control group withmaximum values of 1.44 and 2.34 μg/L (PN + P + Fe < 0.05), respectively. Both of these peak values were lower
than those for the N + P and N + P + Fe groups at stations A3 and A6. The Chl a peaks in the N + P and
N + P + Fe groups both appeared on day 4, which was 2 to 3 days earlier than at the other two stations.
As at stations A3 and A6, Chl a in the N group (PN < 0.05) showed a slowly increasing pattern and reacheda maximum (0.86 μg/L) on the last incubation day. In the dust group, Chl a (PDust < 0.05) showed a maximum
concentration of 0.78 μg/L on day 5. However, different from the responses at stations A3 and A6, both the P
and rainwater groups showed positive responses of Chl a with peaks of 0.77 and 0.82 μg/L, respectively, ondays 4 and 5.
Nutrients at station WG2 (Figure 3) decreased markedly in the N, N + P, and N + P + Fe groups. When reaching
the maximum Chl a during incubation, DIN concentration dropped to 8%, 6%, and 5% of the initial values in
the N, N + P, and N + P + Fe groups, respectively. In the N group, DIP ﬂuctuated at an extremely low concentration (9–15 nmol/L), which was the same as that at stations A3 and A6. DIN in P group showed a low
concentration during the incubation period. Nutrients in the dust group also decreased despite having low
initial values. In the rainwater group, both DIN and DIP exhibited low concentrations, while silicate showeda marked decrease from 2.2 to 0.67 μmol/L. The decrease in silicate in the control group was also the sameas that observed at stations A3 and A6.
3.3.2. Phytoplankton Community
At station WG2, the phytoplankton community included diatoms and dinoﬂagellates with a proportion of
30.5% and 69.5%, respectively, in algae abundance (Table 6). The low total abundance of 0.37 × 104 cells/L
was consistent with the low background Chl a concentration. After the ﬁrst 4 days of incubation, Nitzschia
spp. became the dominant species with a proportion over 50% in all eight groups. On day 4, the abundancein the N + P (105.4 × 104 cells/L) and N + P + Fe groups (64.4 × 104 cells/L) was higher than in other groups,
which was also consistent with the observed higher Chl a peak. The dust group was not an exception with
Nitzschia spp. being dominant during the bloom. After the bloom period, the phytoplankton communities
showed slightly different succession trends in different groups, as was observed at station A3. Speciﬁcally,
Chaetoceros spp. became the dominant species on days 7 and 9 in the N group; dinoﬂagellates were dominant on day 7 in the N + P group; Leptocylindrus spp. became dominant on day 9 in the P group. In othergroups, Nitzschia spp. was dominant from day 4 to the end of the incubation.

4. Discussion
4.1. Nutrient Limitation in the SCS
Nutrient enrichment experiments are a well-utilized methodology for evaluating nutrient limitation in different ocean biota (Moore et al., 2013). In our in situ incubation experiments, N groups at all three stations
showed a positive but slow Chl a response (Figure 2). However, almost all groups with the addition of phosphorus or iron alone showed no obvious Chl a response, which is indicative of nitrogen limitation in the SCS.
Previous research also showed similar results and suggested that nitrogen plays the critical role in the SCS(Chen, 2005; Guo et al., 2012; Wu et al., 2003).

CHU ET AL.

8

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Compared to N groups, Chl a in N + P and N + P + Fe groups at all three stations showed faster increaseand higher peaks, suggesting that phosphorus is also a limiting nutrient for the algae in nitrogen-enriched
condition. Other studies also showed a more strongly positive Chl a response to N + P addition than to theaddition of N + Si or P + Si (Guo et al., 2012). These ﬁndings were consistent with the in situ studies in thetropical Atlantic (Davey et al., 2008; Moore et al., 2008), that low-latitude surface ocean waters were
universally limited by nitrogen with phosphorus being a secondary liming nutrient (Moore et al., 2013).
Iron was not considered to be a strongly limiting element from our experiments as almost no Chl a
response to the addition of iron alone was found. Chen (2005) also found no apparent Chl a responseto the addition of iron alone by incubation experiments, although Wu et al. (2003) inferred the importanceof iron on N2 ﬁxation process by algae. Previous research indicated that iron mostly limited the highnutrient low-chlorophyll regions (Boyd et al., 2000; Tsuda et al., 2003) at high latitude. But for the lownutrient low-chlorophyll regions such as the SCS, the promotion effect of iron on the ecosystem was
not apparent. Overall, nitrogen and phosphorus were both urgently needed by phytoplankton in the
SCS and the region was more likely to be nitrogen limited.
4.2. Phytoplankton Community Succession
In the SCS, all sized (pico-sized, nano-sized, and micro-sized) phytoplankton existed in surface seawater. With
more nutrient supplementation, the abundance of micro-sized algae such as diatoms would apparently
increase (Chen, 2005). In this study, we used the identiﬁcation results by inverted microscope to investigate
the variation of phytoplankton community during the incubation period.
Our experiments showed a similar evolution of the algae community at all three stations that diatoms
became the dominant algae in apparent Chl a-increased groups (e.g., in N + P and N + P + Fe groups)(Tables 4–6). This dominance occurred no matter whether the dominant algae at the start of the experiments
were diatoms (at stations A3 and A6) or dinoﬂagellates (at station WG2). These results were consistent withthose of previous study that diatoms had an advantage in growth competition under nutrient-enriched
conditions (Boyd et al., 2007; Chen et al., 2004; Guo et al., 2012). High growth rates of micro-sized algae
coupled with low grazing pressure from zooplankton in nutrient-enriched condition was probably the reasonof competitive advantage of micro-sized algae (Landry et al., 2000).
Furthermore, Chaetoceros spp. became the dominant diatom species during the bloom period in apparent
Chl a-increased groups at stations A3 and A6, while Nitzschia spp. was the dominant diatom species at station
WG2. Chen (2005) also reported that Chaetoceros spp. and Nitzschia spp. would become the dominant diatom
species with more nutrient supplement in surface seawater in the SCS. After the bloom period in the incubation, the dominant algae changed to other diatom species (e.g., Leptocylindrus spp. or Licmophora spp.) or
dinoﬂagellate (Tables 4 and 6) in most of the groups.
Changes in phytoplankton community in the presence of dust addition nearly mirrored those in N + P or
N + P + Fe groups, with Chaetoceros spp. becoming the dominant species at stations A3 and A6, andNitzschia spp. became dominant at station WG2. Other research conducted in different regions also showedsimilar results, such as that of showing the induction of increased abundance of diatoms by Saharan dust
(Franchy et al., 2013). Some incubation studies also produced different results, such as a response frompico-sized phytoplankton for the ﬁrst addition of dust, while all phytoplankton sizes show a positive responseto the second addition (Giovagnetti et al., 2013). The negative response of micro-sized phytoplankton to dust
addition was also reported in some studies (Herut et al., 2005).
As phytoplankton growth had a close relation with microzooplankton (e.g., nanoﬂagellates and ciliates)
grazing in the oligotrophic SCS (Chen et al., 2009), microzooplankton could exist in our incubation systems
and grew with sufﬁcient food and less mesozooplankton control (Guo et al., 2012; Romero et al., 2011).
However, the Chl a and algae community should not suffer much from microzooplankton grazing in the early
incubation period, which is also suggested by another study (Giovagnetti et al., 2013). Another factor wasbacteria that fed on dissolved organic carbon, which could also affect material ﬂow in the incubation system.
Thus, the algae community pattern after the bloom had some uncertainty under the effects of several marineorganisms and biogeochemical processes.
In addition to the dominant condition in phytoplankton community during the incubation, the variation of
species diversity was also estimated by using Shannon Index (Shannon & Weaver, 1949; Spellerberg &CHU ET AL.

9

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

P 
Fedor, 2003) H ¼  Si¼1 nNi  log2 nNi , where ni was the quantity of a speciﬁc species, N was the total quantity of all species, and S was species richness. From the results, lower Shannon Index values were found in the Chl abloom period (~4–8 days) compared with initial values on day 0 (Figure 4).
During the bloom, in apparent Chl a increase groups like N + P or
N + P + Fe groups, the Shannon Index was generally lower than those incontrol groups that showed unapparent Chl a increase. The results indicated that species diversity would decrease when Chl a concentration
increased. Such phenomenon was also reported in previous research inwhich species diversity would decrease when phytoplankton biomass
reached a high level (Irigoien et al., 2004). After the bloom, the species
diversity showed a slightly increasing trend indicated by higher Shannon
Index in some groups on day 12 (at station A3) and day 9 (at station
WG2). The dust also showed similar effect on species diversity variation
with lower Shannon Index compared to control. The overall results
indicated that species diversity would ﬁrst decrease and then increaseduring the incubation experiments, in contrast to the Chl a variation
pattern.
4.3. Possible Existence of DOP Utilization
The obvious increase of Chl a and the low concentration of DIP in N groups
at all three stations implied another source of phosphorus assimilated byphytoplankton. The phenomenon would be clearer by the imbalance ofthe decreased DIP in incubation seawater and the phosphorus requiredby increased Chl a. Here a Phosphorus Requirement Index (PRI) was proposed as below:
PRI ¼

Prequired –Pdecreased
Prequired

Prequired ¼ ΔChl a · Rc=chla · Redfield P=C
Pdecreased ¼ ΔDIP

Figure 4. Shannon Index H of all incubation groups at stations A3, A6, andWG2.

where ΔChl a was the difference of Chl a in its peak day and 0 day, andΔDIP was the difference of DIP in Chl a peak day and 0 day. We used a ﬁxed
Rc/chla = 50 gC/(g Chl a) (Moll, 1998), and Redﬁeld ratio of C/P = 106/1 in thecalculation. The positive PRI value meant that the system did not supply
sufﬁcient DIP for increasing Chl a. The negative value meant the oversupplement of DIP for Chl a increasing, which indicated the luxury DIP
assimililation by phytoplankton during the incubation.

As presented in Figure 5, the PRI in N groups was higher than almost all theother groups, which strongly implied the presence of other undetected phosphorus sources in our experiments. The values in P groups were lowest at each station, which indicated oversupplements of DIP.
Although the PRI value did not exactly reﬂect the accurate phosphorus demand with variable element
stoichiometry in algae cells, the decreasing PRI trend in different groups and the higher values in N group stillreasonably conﬁrmed the undetected phosphorus in N groups. In addition, the Chl a increase in N groups
showed a unique smooth increasing trend at all three stations (Figure 2), which also implied the slow assimilation of other phosphorus sources. DOP and particulate phosphorus are two possible candidates of theunknown phosphorus. However, with low remineralization rate and also low concentration of particles in
the SCS (Hung et al., 2007), particulate phosphorus was not a likely possible source. On the other hand,previous research on phosphate assimilation showed that DOP was an important phosphorus source contributing to the growth of phytoplankton in oligotrophic areas (Lomas et al., 2010; Reynolds et al., 2014).
Therefore, we assumed that DOP was used in the incubation experiments.
To conﬁrm the source of phosphorus in N groups and also better realize the biological process, a biogeochemical box model with nutrients, phytoplankton, and detritus (called NPD model) (Moll, 1998; Skogen

CHU ET AL.

10

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

et al., 1995; Zhao & Guo, 2011) was applied to simulate our incubation
experiments. The model equations and conﬁgurations are shown in
Tables S1–S4 in the supporting information, and parameters referred toin previous studies (Broekhuizen et al., 1995; Chai et al., 2002; Duarte
et al., 2003; Moll, 1998; Redﬁeld, 1958; Tian et al., 2005; Zhao & Guo,
2011; Zhao et al., 2002) are shown in Table S5 in the supporting information. We found that in some groups, especially N groups, the modeled
results underestimated the Chl a (Figure 5), mainly due to P limitation.
The results also conﬁrmed the necessity of another source of phosphorus.
To examine whether the DOP utilization can improve the model results, a
simple phosphorus back-calculation scheme (shortened for PBS) based on
Figure 5. The Phosphorus Requirement Index (PRI) in different incubation
DOP utilization mechanism was proposed. Mahaffey et al. (2014) reported
groups at station A3 (squares), station A6 (triangles) and station WG2that when DIP decreased below 0.03 μmol/L, DOP would be possibly used.
(circles).
Using 0.068 μmol/L (Table S5) as the value of DIP half-saturation constant,the limiting coefﬁcient rDIP (Table S2) would become lower than 0.3 when DIP concentration decreased below
0.03 μmol/L. Thus, when rDIP was lower than 0.3 and also became the minimum of the nutrient-limiting coefDIP K DIP
ﬁcient (Table S2), we kept rDIP equal to 0.3, and then DIP would be recalculated as DIP ¼ r1:0r. The differDIP
ence of DIP value before and after trigging the scheme represented the utilized DOP concentration. A up
limit of DOP stock that can be used in the incubation bottle was also given in the scheme, estimated by
3.35-fold of initial DIP stock (Karl & Yanagi, 1997) in control group at each station.
After embedding the scheme, seven groups triggered the PBS (Figure 6) in the model. With PBS, the simulated Chl a showed a good ﬁtting with measured values. In the three N groups, the modeled results all reproduced the slowly increasing trend of Chl a, despite a higher modeled peak at station A3 (Figure 6). In the twodust groups at stations A6 and WG2, the simulated Chl a showed a reasonable increase. However, the model
did not reproduce the early appearance of the Chl a peak in the two dust groups. In addition, the slightincrease of Chl a in control and rainwater groups at station A6 was also well reproduced by the modelwith PBS.
4.4. Promotion Effect of Dust Input in the SCS
The dust promotion effect on phytoplankton bloom has been widely reported (Giovagnetti et al., 2013;
Ridame & Guieu, 2002), and the SCS was not an exception (Tan et al., 2011; Wang et al., 2012). Our incubation
experiments in the region also showed a positive Chl a response to dust addition with the Chl a peak in dustgroups being 2.1-fold, 1.4-fold, and 2.6-fold of those in the control incubation at stations A3, A6, and WG2(Figure 2), respectively. The amount of phosphorus and iron that leached from the dust sample was extremely low in our experiments (Table 2). Thus, nitrogen was inferred to be the critical nutrient that promoted

Figure 6. Measured Chl a (dots), simulated Chl a with phosphorus back-calculation scheme (PBS) (dashed lines) and without PBS (solid lines). At station A3, (a) Ngroup; at station A6, (b) control group, (c) N group, (d) dust group and (e) rainwater group; and at station WG2, (f) N group and (g) dust group.

CHU ET AL.

11

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

phytoplankton growth. The model results also showed that with the single addition of nitrogen from dust,
simulated Chl a showed almost the same increasing trend for the addition of both nitrogen and phosphorus(Figure S1). The promotion effect in in situ experiments by Guo et al. (2012) was conﬁrmed in our research aswell, despite the fact that the aerosol in their experiment was not collected during the dust storm season.
In addition to the stimulative effect for algae blooms, the incubation experiments in the dust groups also
showed a slight increase in algae growth rate, which could be known from the shorter time for Chl a to peakin dust groups compared to other groups at stations A3 and A6. The Chl a peak in dust groups appeared on
day 5 of the incubation at all three stations. At stations A3 and A6, Chl a reached a peak on day 6 in N + P + Fe
groups (Figure 2), while the peak in N + P groups was on day 7. Thus, the addition of multiple bioavailable
elements by dust likely shortened the response time of Chl a in our experiments. These results were reasonable as trace metals were necessary for algae growth and metabolism (Wolfe-Simon et al., 2005).
Furthermore, in dust groups at stations A6 and WG2, the model with DOP utilization scheme well simulated
the increase of Chl a but failed to reproduce the early appearance of the peak (Figure 6). The results inferredthat dust might show the capacity of enhancing the transformation and assimilation of DOP, which then led
to the higher growth rate of algae. Previous research also reported the importance of trace metals to alkaline
phosphatase activity and then to DOP utilization (Kim & Wyckoff, 1991; McComb et al., 1979). In situ experiments also showed that trace metals like zinc could increase the alkaline phosphatase activity rate in the
Atlantic Ocean (Mahaffey et al., 2014). Thus, it is reasonable to infer that trace metals in the dust could raise
the growth rate by accelerating DOP transformation. As the Chl a peak time in the dust group at station WG2
was later than in the N + P and N + P + Fe groups, the acceleration for DOP utilization might also have an
upper limit.
As our dust sampling place was located almost at the end place before Asian dust leaves the continent, thedust sample was representative of the dust deposited in the marginal seas. But during long-distance transportation, the aerosol composition could be affected by the local environment. The amounts of nutrients likeparticulate NO3 and NH4+ in our dust sampling place were higher than those collected in the SCS (Qi et al.,2018; Zhang et al., 2007), which was also true for trace metals, especially for Fe (Table S6). Thus, our experiments had a possibility to overestimate the promotion effect by Asian dust.
4.5. Different Responses in Oligotrophic and Ultraoligotrophic Regions
In the world ocean, oligotrophic areas are distributed mostly in the low-latitude region. Among them, someregions showed even more oligotrophic conditions, for example, at eastern Mediterranean and South Paciﬁcgyre (Moutin et al., 2017; Thingstad et al., 2005). Although there was no speciﬁc deﬁnition to classify oligotrophic and ultraoligotrophic conditions, Moutin et al. (2012) indicated that the ultraoligotrophic regions
show a deeper nitracline depth and lower primary production in the eastern Mediterranean. Thingstad
et al. (2005) conﬁrmed the ultraoligotrophic status with low surface Chl a concentration (0.02 μg/L) and extremely low nutrient concentration near detection limit in the eastern Mediterranean.
In our study, WG2 station possibly represented the ultraoligotrophic condition with nutrient concentrations
close to detection limit and the initial Chl a also at a low level of 0.04 μg/L (Table 1). For the phytoplankton
community, diatoms dominated the phytoplankton community at stations A3 and A6 while dinoﬂagellates
were dominant at station WG2, which was consistent with previous research (Chen, 2005) that showed that
small-sized algae dominated the community in regions with extremely low nutrients in the SCS. Previous
studies indicated that the combination of the Kuroshio intrusion, ocean circulation, and eddies generated
upwelling in the northern SCS (Shang et al., 2012; Shaw et al., 1996; Xiu & Chai, 2011). Since our samplingstations were near an upwelling center located about 100 km northwest off Luzon Island (Liu et al., 2002),
the slightly higher nutrients and Chl a at stations A3 and A6 might be due to the upwelling.
In ultraoligotrophic environment, the Chl a response showed different characters in some incubation groups
at station WG2, compared to those at stations A3 and A6. At station WG2, the incubation system exhibited afaster phytoplankton growth in response to both nitrogen- and phosphorus-enriched environment,
indicated by the earlier appearance of the Chl a peak in N + P and N + P + Fe groups (on day 4) than corresponding groups (on day 6 or 7) at stations A3 and A6. Also, in the modeling, a higher maximum growth rate
(Table S5) was needed when simulating the incubations at station WG2 in order to reproduce the early
appearance of Chl a peaks.

CHU ET AL.

12

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Interestingly, the single addition of phosphorus promoted extra phytoplankton growth only at station WG2(Figure 2). Under extremely low nitrogen concentration (0.1 μmol/L) in background seawaters at station WG2,
the Chl a in P group at station WG2 suggested that phytoplankton communities might have initiated somemechanisms to relieve the stress of depleted DIN. And previous research also reported the existence andimportance of N2 ﬁxation processes in the SCS (Chen, 2005; Chen et al., 2014; Wu et al., 2003). As the incubation seawater was ﬁltered through nylon mesh at the beginning of the experiments, the N2 ﬁxation
conducted by diazotroph Trichodesmium spp. which always gathered in clusters might be weakened. And
at station WG2, N2 ﬁxation might be mainly conducted by unicellular diazotrophs, which was reported dominating the N2 ﬁxation process in ultraoligotrophic regions (Moutin et al., 2017). For the P group at station
WG2, since N2 ﬁxation was easily constrained by availability of DIP or Fe, or both (Capone, 2001; Mills et al.,
2004; Sanudo-Wilhelmy et al., 2001), the abundant phosphate in the P group might lead to the promotionof N2 ﬁxation processes and further lead to Chl a increase.
Rainwater deposition is an important input of multiple nutrients and trace metals to the ocean (Duce et al.,
1991; Jung et al., 2013), though in situ researches were scarce. In a previous study in the SCS, Cui et al.
(2016) reported the slightly positive Chl a response to rainwater deposition in incubation experiments.
From our experiment, the response in the rainwater groups was different in the two different regions in
the SCS. The Chl a responses were slight at stations A3 and A6, compared with the apparent positive responseat station WG2. The slight response possibly resulted from assimilation of background nutrients at stations A3
and A6, as the Chl a in control groups also showed a similar slight increase at the two stations. But at station
WG2, DOP utilization and N2 ﬁxation might both exist, which contributed to the Chl a increase in the rainwater group. Trace metals in the rainwater might have strengthened the two processes leading to the more
apparent Chl a increase over that of the control at station WG2.

5. Conclusion
To evaluate marine ecosystem responses to atmospheric forcing, especially dust deposition in the SCS, we
conducted onboard incubation experiments with surface seawater sampled at three stations. The entire
process including bloom and recession were shown in the different incubation groups with nutrients (nitrogen, phosphorus, and iron), dust, and rainwater additions. At all three stations, the addition of nitrogen alone,rather than addition of phosphorus or iron alone, showed a stimulatory effect on phytoplankton growth, indicating that nitrogen is the most critical nutrient in the SCS. Since the N + P and N + P + Fe groups showed aneven higher Chl a peak than the N group, phosphorus could be the secondary limiting nutrient. Under such
nutrient condition in the SCS, dust showed an apparent promotion effect on phytoplankton growth byproviding sufﬁcient nitrogen. The early appearance of the Chl a peak in dust groups also indicated the abilityof increasing algae growth rate by dust, probably due to trace metals leaching from the dust.
During the incubation, the ecosystem showed a succession in phytoplankton community. The initial ecosystem was dominated by either diatoms or dinoﬂagellates, and diatoms became the dominant algae during thebloom period in nutrient-enriched environments (e.g., in N + P, N + P + Fe, and dust groups). Nitzschia spp.
and Chaetoceros spp. were the dominant species of diatoms. The community succession showed no apparent
difference between dust group and N + P as well as N + P + Fe groups. Our results indicated the possibility
that the algae community would change under external nutrient addition.
In our incubation experiments, N groups at all three stations showed a positive response and slowly increasing trend of Chl a in the condition of DIP deﬁciency. The high PRI values in N groups conﬁrmed the undetected source of phosphorus. Also, from model perspective, after embedding a PBS scheme, the model
results can better reproduce the Chl a increasing pattern in N groups and also some other groups. From bothexperimental and model perspectives, we proposed the possible existence of DOP utilization by the algae in
the SCS.
In addition, different initial condition in background seawater indicated the possible presence of oligotrophic(stations A3 and A6) and ultraoligotrophic (station WG2) regions in the SCS. At the ultraoligotrophic station
WG2, Chl a and nutrient concentrations were extremely low, while Chl a showed faster response to abundantnutrient addition (e.g., N + P and N + P + Fe groups) with a higher algae growth rate. The dominant algae atstation WG2 changed from dinoﬂagellates to diatoms, and Nitzschia spp. was the dominant diatom species

CHU ET AL.

13

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

during the bloom period. On the other hand, the dominant algae at stations A3 and A6 were always diatoms
in which Chaetoceros spp. was dominant. The positive response of Chl a in the P group at station WG2 impliedthat other bioavailable nitrogen sources might exist, for example, N2 ﬁxation, since the background DIN in theseawater was scarce. Rainwater groups at station WG2 also showed a positive Chl a response, but those atstations A3 and A6 did not. As rainwater provided little added nutrients, N2 ﬁxation and DOP utilization
processes might both have contributed to the algae growth.
Acknowledgments
The authors gratefully acknowledge
Jinhui Shi and Xiaohuan Liu at Ocean
University of China for their help in the
incubation experiments and Yan Li at
First Institute of Oceanography for thehelp in phytoplankton community
identiﬁcation. This work is funded by
the National Nature Science Foundationof China (41210008), the National Key
Basic Research Program of China(2014CB953700) and the NSFCShandong Joint Fund for Marine
Ecology and Environmental Sciences(U1606404). Qiang Chu thanks the
China Scholarship Council (CSC) for
supporting his stay in Japan. Xinyu Guo
thanks support of the Fundamental
Research Funds for Central Universitiesof the Ministry of Education of China
under the contract 201512004.
Huiwang Gao is thankful for the support
by the Ministry of Education, Culture,
Sports, Science and Technology, Japan(MEXT) to a project on Joint
Usage/Research Center-Leading
Academia in Marine and Environment
Pollution Research (LaMer). The data
used in this study are provided in theﬁles in the supporting information andalso available upon request to the corresponding author.

CHU ET AL.

References
Al-Momani, I. F. (2003). Trace elements in atmospheric precipitation at Northern Jordan measured by ICP-MS: Acidity and possible sources.
Atmospheric Environment, 37(32), 4507–4515. https://doi.org/10.1016/S1352-2310(03)00562-4
Arrigo, K. R. (2005). Marine microorganisms and global nutrient cycles. Nature, 437(7057), 349–355. https://doi.org/10.1038/nature04159
Boyd, P. W., Watson, A. J., Law, C. S., & Abraham, E. R. (2000). A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated byiron fertilization. Nature, 407(6805), 695–702. https://doi.org/10.1038/35037500
Boyd, P. W., Jickells, T., Law, C. S., Blain, S., Boyle, E. A., Buesseler, K. O., et al. (2007). Mesoscale iron enrichment experiments 1993–2005:
Synthesis and future directions. Science, 315(5812), 612–617. https://doi.org/10.1126/science.1131669
Broekhuizen, N., Heath, M. R., Hay, S. J., & Gurney, W. S. C. (1995). Modelling the dynamics of the North Sea’s mesozooplankton. Netherlands
Journal of Sea Research, 33(3-4), 381–406. https://doi.org/10.1016/0077-7579(95)90054-3
Capone, D. G. (2001). Marine nitrogen ﬁxation: What’s the fuss? Current Opinion in Microbiology, 4(3), 341–348. https://doi.org/10.1016/
S1369-5274(00)00215-0
Chai, F., Dugdale, R. C., Peng, T. H., Wilkerson, F. P., & Barber, R. T. (2002). One-dimensional ecosystem model of the equatorial Paciﬁc
upwelling system. Part I: Model development and silicon and nitrogen cycle. Deep Sea Research Part II: Topical Studies in Oceanography,
49(13-14), 2713–2745. https://doi.org/10.1016/S0967-0645(02)00055-3
Chen, Y.-L. L. (2005). Spatial and seasonal variations of nitrate-based new production and primary production in the South China Sea. Deep
Sea Research Part I: Oceanographic Research Papers, 52(2), 319–340. https://doi.org/10.1016/j.dsr.2004.11.001
Chen, Y.-L. L., & Chen, H.-Y. (2006). Seasonal dynamics of primary and new production in the northern South China Sea: The signiﬁcance ofriver discharge and nutrient advection. Deep Sea Research Part I: Oceanographic Research Papers, 53(6), 971–986. https://doi.org/10.1016/j.
dsr.2006.02.005
Chen, Y.-L. L., Chen, H.-Y., Karl, D. M., & Takahashi, M. (2004). Nitrogen modulates phytoplankton growth in spring in the South China Sea.
Continental Shelf Research, 24(4-5), 527–541. https://doi.org/10.1016/j.csr.2003.12.006
Chen, B., Liu, H., Landry, M. R., DaI, M., Huang, B., & Sune, J. (2009). Close coupling between phytoplankton growth and microzooplankton
grazing in the western South China Sea. Limnology and Oceanography, 54(4), 1084–1097. https://doi.org/10.4319/lo.2009.54.4.1084
Chen, Y.-L. L., Chen, H.-Y., Lin, Y.-H., Yong, T.-C., Taniuchi, Y., & Tuo, S.-h. (2014). The relative contributions of unicellular and ﬁlamentous
diazotrophs to N2 ﬁxation in the South China Sea and the upstream Kuroshio. Deep Sea Research Part I: Oceanographic Research Papers, 85,
56–71. https://doi.org/10.1016/j.dsr.2013.11.006
Cui, D.-Y., Wang, J.-T., Tan, L.-J., & Dong, Z.-Y. (2016). Impact of atmospheric wet deposition on phytoplankton community structure in theSouth China Sea. Estuarine, Coastal and Shelf Science, 173, 1–8. https://doi.org/10.1016/j.ecss.2016.02.011
Davey, M., Tarran, G. A., Mills, M. M., Ridame, C., Geider, R. J., & LaRoche, J. (2008). Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic. Limnology and Oceanography, 53(5), 1722–1733. https://doi.org/10.4319/
lo.2008.53.5.1722
Duarte, P., Meneses, R., Hawkins, A. J. S., Zhu, M., Fang, J., & Grant, J. (2003). Mathematical modelling to assess the carrying capacity for multispecies culture within coastal waters. Ecological Modelling, 168(1-2), 109–143. https://doi.org/10.1016/S0304-3800(03)00205-9
Duce, R. A., Liss, P. S., Merrill, J. T., Atlas, E. L., Buat-Menard, P., Hicks, B. B., et al. (1991). The atmospheric input of trace species to the world
ocean. Global Biogeochemical Cycles, 5(3), 193–259. https://doi.org/10.1029/91GB01778
Duce, R. A., LaRoche, J., Altieri, K., Arrigo, K. R., Baker, A. R., Capone, D. G., et al. (2008). Impacts of atmospheric anthropogenic nitrogen on the
open ocean. Science, 320(5878), 893–897. https://doi.org/10.1126/science.1150369
Eppley, R. W., & Peterson, B. J. (1979). Particulate organic matter ﬂux and planktonic new production in the deep ocean. Nature, 282(5740),
677–680. https://doi.org/10.1038/282677a0
Franchy, G., Ojeda, A., López-Cancio, J., & Hernández-León, S. (2013). Plankton community response to Saharan dust fertilization in subtropical waters off the Canary Islands. Biogeosciences Discussions, 10(11), 17,275–17,307. https://doi.org/10.5194/bgd-10-17275-2013
Gao, Y., Arimoto, R., Duce, R. A., Zhang, X.-Y., Zhang, G.-Y., An, Z.-S., et al. (1997). Temporal and spatial distributions of dust and its deposition
to the China Sea. Tellus Series B: Chemical and Physical Meteorology, 49(2), 172–189. https://doi.org/10.3402/tellusb.v49i2.15960
Giovagnetti, V., Brunet, C., Conversano, F., Tramontano, F., Obernosterer, I., Ridame, C., & Guieu, C. (2013). Assessing the role of dust
deposition on phytoplankton ecophysiology and succession in a low-nutrient low-chlorophyll ecosystem: A mesocosm experiment in the
Mediterranean Sea. Biogeosciences, 10(5), 2973–2991. https://doi.org/10.5194/bg-10-2973-2013
Guo, C., Yu, J., Ho, T. Y., Wang, L., Song, S., Kong, L., & Liu, H. (2012). Dynamics of phytoplankton community structure in the South China Sea
in response to the east Asian aerosol input. Biogeosciences, 9(4), 1519–1536. https://doi.org/10.5194/bg-9-1519-2012
Herbland, A., Le Bouteiller, A., & Raimbault, P. (1985). Size structure of phytoplankton biomass in the equatorial Atlantic Ocean. Deep Sea
Research Part A: Oceanographic Research Papers, 32(7), 819–836. https://doi.org/10.1016/0198-0149(85)90118-9
Herut, B., Zohary, T., Krom, M. D., Mantoura, R. F. C., Pitta, P., Psarra, S., et al. (2005). Response of East Mediterranean surface water to Saharandust: On-board microcosm experiment and ﬁeld observations. Deep Sea Research Part II: Topical Studies in Oceanography, 52(22-23),
3024–3040. https://doi.org/10.1016/j.dsr2.2005.09.003
Hsu, S.-C., Wong, G. T. F., Gong, G. C., Shiah, F. K., Huang, Y. T., Kao, S. J., et al. (2010). Sources, solubility, and dry deposition of aerosol traceelements over the East China Sea. Marine Chemistry, 120(1-4), 116–127. https://doi.org/10.1016/j.marchem.2008.10.003
Hung, J.-J., Wang, S.-M., & Chen, Y.-L. (2007). Biogeochemical controls on distributions and ﬂuxes of dissolved and particulate organic carbon
in the northern South China Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 54(14-15), 1486–1503. https://doi.org/10.1016/
j.dsr2.2007.05.006
Irigoien, X., Huisman, J., & Harris, R. P. (2004). Global biodiversity patterns of marine phytoplankton and zooplankton. Nature, 429(6994),
863–867. https://doi.org/10.1038/nature02593

14

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Jickells, T. D., An, Z. S., Andersen, K. K., Baker, A. R., Bergametti, G., Brooks, N., et al. (2005). Global iron connections between desert dust, ocean
biogeochemistry, and climate. Science, 308(5718), 67–71. https://doi.org/10.1126/science.1105959
Jung, J., Furutani, H., Uematsu, M., Kim, S., & Yoon, S. (2013). Atmospheric inorganic nitrogen input via dry, wet, and sea fog deposition to thesubarctic western North Paciﬁc Ocean. Atmospheric Chemistry and Physics, 13(1), 411–428. https://doi.org/10.5194/acp-13-411-2013
Karl, D. M., & Yanagi, K. (1997). Partial characterization of the dissolved organic phosphorus pool in the oligotrophic North Paciﬁc Ocean.
Limnology and Oceanography, 42(6), 1398–1405. https://doi.org/10.4319/lo.1997.42.6.1398
Kim, E. E., & Wyckoff, H. W. (1991). Reaction mechanism of alkaline phosphatase based on crystal structures. Journal of Molecular Biology,218(2), 449–464. https://doi.org/10.1016/0022-2836(91)90724-K
Landry, M. R., Constantinou, J., Latasa, M., Brown, S. L., Bidigare, R. R., & Ondrusek, M. E. (2000). Biological response to iron fertilization in theeastern equatorial Paciﬁc (IronEx II). III. Dynamics of phytoplankton growth and microzooplankton grazing. Marine Ecology Progress Series,
201, 57–72. https://doi.org/10.3354/meps201057
Lin, X., Zhang, H., Huang, B.-Q., & Lin, S.-J. (2012). Alkaline phosphatase gene sequence characteristics and transcriptional regulation byphosphate limitation in Karenia brevis (Dinophyceae). Harmful Algae, 17, 14–24. https://doi.org/10.1016/j.hal.2012.02.005
Liu, K.-K., Chao, S.-Y., Shaw, P.-T., Gong, G.-C., Chen, C.-C., & Tang, T.-Y. (2002). Monsoon-forced chlorophyll distribution and primary production in the South China Sea: Observations and a numerical study. Deep Sea Research Part I: Oceanographic Research Papers, 49(8),1387–1412. https://doi.org/10.1016/S0967-0637(02)00035-3
Liu, Y., Zhang, T.-R., Shi, J.-H., Gao, H.-W., & Yao, X.-H. (2013). Responses of chlorophyll a to added nutrients, Asian dust, and rainwater in an
oligotrophic zone of the Yellow Sea: Implications for promotion and inhibition effects in an incubation experiment. Journal of GeophysicalResearch: Biogeosciences, 118, 1763–1772. https://doi.org/10.1002/2013JG002329
Lomas, M. W., Burke, A. L., Lomas, D. A., Bell, D. W., Shen, C., Dyhrman, S. T., & Ammerman, J. W. (2010). Sargasso Sea phosphorus biogeochemistry: An important role for dissolved organic phosphorus (DOP). Biogeosciences, 7(2), 695–710. https://doi.org/10.5194/bg-7695-2010
Mahaffey, C., Reynolds, S., Davis, C. E., & Lohan, M. C. (2014). Alkaline phosphatase activity in the subtropical ocean: Insights from nutrient,dust and trace metal addition experiments. Frontiers in Marine Science, 1(73), 1–13. https://doi.org/10.3389/fmars.2014.00073
McComb, R. B., Bowers, G. N. Jr., & Posen, S. (1979). Alkaline phosphatase. New York: Plenum Press. https://doi.org/10.1007/978-1-4613-2970-1
Mills, M. M., Ridame, C., Davey, M., La Roche, J., & Geider, R. J. (2004). Iron and phosphorus co-limit nitrogen ﬁxation in the eastern tropicalNorth Atlantic. Nature, 429(6989), 292–294. https://doi.org/10.1038/nature02550
Moll, A. (1998). Regional distribution of primary production in the North Sea simulated by a three-dimensional model. Journal of Marine
Systems, 16(1-2), 151–170. https://doi.org/10.1016/S0924-7963(97)00104-8
Moore, C. M., Mills, M. M., Langlois, R., Milne, A., Achterberg, E. P., La Roche, J., & Geider, R. J. (2008). Relative inﬂuence of nitrogen andphosphorous availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean. Limnology
and Oceanography, 53(1), 291–305. https://doi.org/10.4319/lo.2008.53.1.0291
Moore, C. M., Mills, M., Arrigo, K., Berman-Frank, I., Bopp, L., Boyd, P., et al. (2013). Processes and patterns of oceanic nutrient limitation. Nature
Geoscience, 6(9), 701–710. https://doi.org/10.1038/ngeo1765
Moutin, T., Van Wambeke, F., & Prieur, L. (2012). Introduction to the Biogeochemistry from the Oligotrophic to the Ultraoligotrophic
Mediterranean (BOUM) experiment. Biogeosciences, 9(10), 3817–3825. https://doi.org/10.5194/bg-9-3817-2012
Moutin, T., Doglioli, A. M., de Verneil, A., & Bonnet, S. (2017). Preface: The Oligotrophy to the UlTra-oligotrophy PACiﬁc Experiment (OUTPACE
cruise, 18 February to 3 April 2015). Biogeosciences, 14(13), 3207–3220. https://doi.org/10.5194/bg-14-3207-2017
Qi, J., Liu, X., Yao, X., Zhang, R., Chen, X., Lin, X., et al. (2018). The concentration, source and deposition ﬂux of ammonium and nitrate inatmospheric particles during dust events at a coastal site in northern China. Atmospheric Chemistry and Physics, 18(2), 571–586. https://doi.
org/10.5194/acp-18-571-2018
Redﬁeld, A. C. (1958). The biological control of chemical factors in the environment. American Scientist, 46(3), 230A–221A.
Reynolds, S., Mahaffey, C., Roussenov, V., & Williams, R. G. (2014). Evidence for production and lateral transport of dissolved organic phosphorus in the eastern subtropical North Atlantic. Global Biogeochemical Cycles, 28, 805–824. https://doi.org/10.1002/2013GB004801
Ridame, C., & Guieu, C. (2002). Saharan input of phosphate to the oligotrophic water of the open western Mediterranean Sea. Limnology andOceanography, 47(3), 856–869. https://doi.org/10.4319/lo.2002.47.3.0856
Ridame, C., Dekaezemacker, J., Guieu, C., Bonnet, S., L’Helguen, S., & Malien, F. (2014). Contrasted Saharan dust events in LNLC environments:
Impact on nutrient dynamics and primary production. Biogeosciences, 11(17), 4783–4800. https://doi.org/10.5194/bg-11-4783-2014
Romero, E., Peters, F., Marrasé, C., Guadayol, Ò., Gasol, J. M., & Weinbauer, M. G. (2011). Coastal Mediterranean plankton stimulation dynamics
through a dust storm event: An experimental simulation. Estuarine, Coastal and Shelf Science, 93(1), 27–39. https://doi.org/10.1016/j.
ecss.2011.03.019
Sanudo-Wilhelmy, S. A., Kustka, A. B., Gobler, C. J., Hutchins, D. A., Yang, M., Lwiza, K., et al. (2001). Phosphorus limitation of nitrogen ﬁxation
by Trichodesmium in the central Atlantic Ocean. Nature, 411(6833), 66–69. https://doi.org/10.1038/35075041
Shang, S.-L., Li, L., Li, J., Li, Y.-H., Lin, G., & Sun, J. (2012). Phytoplankton bloom during the northeast monsoon in the Luzon Strait bordering theKuroshio. Remote Sensing of Environment, 124, 38–48. https://doi.org/10.1016/j.rse.2012.04.022
Shannon, C. E., & Weaver, W. (1949). The mathematical theory of information.
Shao, Y.-P., Wyrwoll, K.-H., Chappell, A., Huang, J.-P., Lin, Z.-H., McTainsh, G. H., et al. (2011). Dust cycle: An emerging core theme in Earthsystem science. Aeolian Research, 2(4), 181–204. https://doi.org/10.1016/j.aeolia.2011.02.001
Shaw, P.-T., Chao, S.-Y., Liu, K.-K., Pai, S.-C., & Liu, C.-T. (1996). Winter upwelling off Luzon in the northeastern South China Sea. Journal ofGeophysical Research, 101(C7), 16,435–16,448. https://doi.org/10.1029/96JC01064
Shi, J.-H., Gao, H.-W., Zhang, J., Tan, S.-C., Ren, J.-L., Liu, C.-G., et al. (2012). Examination of causative link between a spring bloom anddry/wet deposition of Asian dust in the Yellow Sea, China. Journal of Geophysical Research, 117, D17304. https://doi.org/10.1029/
2012JD017983
Skogen, M. D., Svendsen, E., Berntsen, J., Aksnes, D., & Ulvestad, K. B. (1995). Modelling the primary production in the North Sea using acoupled three-dimensional physical-chemical-biological ocean model. Estuarine, Coastal and Shelf Science, 41(5), 545–565. https://doi.org/
10.1016/0272-7714(95)90026-8
Spellerberg, I. F., & Fedor, P. J. (2003). A tribute to Claude Shannon (1916–2001) and a plea for more rigorous use of species richness, species
diversity and the ‘Shannon-Wiener’ index. Global Ecology and Biogeography, 12(3), 177–179. https://doi.org/10.1046/j.1466822X.2003.00015.x
Stibor, H., Vadstein, O., Diehl, S., Gelzleichter, A., Hansen, T., Hantzsche, F., et al. (2004). Copepods act as a switch between alternative trophic
cascades in marine pelagic food webs. Ecology Letters, 7(4), 321–328. https://doi.org/10.1111/j.1461-0248.2004.00580.x
Strickland, J. D., & Parsons, T. R. (1972). A practical handbook of seawater analysis. Bulletin of Fisheries Research Board of Canada, 167, 201–213.

CHU ET AL.

15

Journal of Geophysical Research: Biogeosciences

10.1002/2017JG004088

Tan, S.-C., Shi, G.-Y., Shi, J.-H., Gao, H.-W., & Yao, X. (2011). Correlation of Asian dust with chlorophyll and primary productivity in the coastal
seas of China during the period from 1998 to 2008. Journal of Geophysical Research, 116, G02029. https://doi.org/10.1029/2010JG001456
Tan, S.-C., Shi, G.-Y., & Wang, H. (2012). Long-range transport of spring dust storms in Inner Mongolia and impact on the China seas.
Atmospheric Environment, 46, 299–308. https://doi.org/10.1016/j.atmosenv.2011.09.058
Thingstad, T. F., Krom, M. D., Mantoura, R. F., Flaten, G. A., Groom, S., Herut, B., et al. (2005). Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science, 309(5737), 1068–1071. https://doi.org/10.1126/science.1112632
Thingstad, T. F., Havskum, H., Zweifel, U. L., Berdalet, E., Sala, M. M., Peters, F., et al. (2007). Ability of a “minimum” microbial food web model toreproduce response patterns observed in mesocosms manipulated with N and P, glucose, and Si. Journal of Marine Systems, 64(1-4), 15–34.
https://doi.org/10.1016/j.jmarsys.2006.02.009
Tian, T., Wei, H., Su, J., & Chung, C. (2005). Simulations of annual cycle of phytoplankton production and the utilization of nitrogen in the
Yellow Sea. Journal of Oceanography, 61(2), 343–357. https://doi.org/10.1007/s10872-005-0045-z
Tsuda, A., Takeda, S., Saito, H., Nishioka, J., Nojiri, Y., Kudo, I., et al. (2003). A mesoscale iron enrichment in the western subarctic Paciﬁc
induces a large centric diatom bloom. Science, 300(5621), 958–961. https://doi.org/10.1126/science.1082000
Van den Meersche, K., Middelburg, J. J., Soetaert, K., van Rijswijk, P., Boschker, H. T. S., & Heip, C. H. R. (2004). Carbon-nitrogen coupling and13
algal-bacterial interactions during an experimental bloom: Modeling a C tracer experiment. Limnology and Oceanography, 49(3),862–878. https://doi.org/10.4319/lo.2004.49.3.0862
Vincent, W. F. (1981). Rapid physiological assays for nutrient demand by the plankton. I. Nitrogen. Journal of Plankton Research, 3(4), 685–697.
https://doi.org/10.1093/plankt/3.4.685
Vitousek, P. M., & Howarth, R. W. (1991). Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry, 13(2), 87–115. https://doi.org/10.1007/bf00002772
Wang, S.-H., Tsay, S. C., Lin, N. H., Hsu, N. C., Bell, S. W., Li, C., et al. (2011). First detailed observations of long-range transported dust over thenorthern South China Sea. Atmospheric Environment, 45(27), 4804–4808. https://doi.org/10.1016/j.atmosenv.2011.04.077
Wang, S.-H., Hsu, N. C., Tsay, S.-C., Lin, N.-H., Sayer, A. M., Huang, S.-J., & Lau, W. K. M. (2012). Can Asian dust trigger phytoplankton blooms in
the oligotrophic northern South China Sea? Geophysical Research Letters, 39, L05811. https://doi.org/10.1029/2011GL050415
Wolfe-Simon, F., Grzebyk, D., Schoﬁeld, O., & Falkowski, P. G. (2005). The role and evolution of superoxide dismutases in algae. Journal of
Phycology, 41(3), 453–465. https://doi.org/10.1111/j.1529-8817.2005.00086.x
Wong, G. T. F., Ku, T.-L., Mulholland, M., Tseng, C.-M., & Wang, D.-P. (2007). The SouthEast Asian Time-series Study (SEATS) and the biogeochemistry of the South China Sea—An overview. Deep Sea Research Part II: Topical Studies in Oceanography, 54(14-15), 1434–1447. https://doi.org/10.1016/j.dsr2.2007.05.012
Wu, J.-F., Chung, S.-W., Wen, L.-S., Liu, K.-K., Chen, Y.-L. L., Chen, H.-Y., & Karl, D. M. (2003). Dissolved inorganic phosphorus, dissolved iron, andTrichodesmium in the oligotrophic South China Sea. Global Biogeochemical Cycles, 17(1), 1008. https://doi.org/10.1029/2002GB001924
Xiu, P., & Chai, F. (2011). Modeled biogeochemical responses to mesoscale eddies in the South China Sea. Journal of Geophysical Research,
116, C10006. https://doi.org/10.1029/2010JC006800
Yuan, W., & Zhang, J. (2006). High correlations between Asian dust events and biological productivity in the western North Paciﬁc.
Geophysical Research Letters, 33, L07603. https://doi.org/10.1029/2005GL025174
Zhang, Y., Sperber, K. R., & Boyle, J. S. (1997). Climatology and interannual variation of the East Asian winter monsoon: Results from the 1979–
95 NCEP/NCAR reanalysis. Monthly Weather Review, 125(10), 2605–2619. https://doi.org/10.1175/1520-0493(1997)125%3C2605:caivot%
3E2.0.co;2
Zhang, X. Y., Zhuang, G. S., Guo, J. H., Yin, K. D., & Zhang, P. (2007). Characterization of aerosol over the northern South China Sea during two
cruises in 2003. Atmospheric Environment, 41(36), 7821–7836. https://doi.org/10.1016/j.atmosenv.2007.06.031
Zhao, L., & Guo, X.-Y. (2011). Inﬂuence of cross-shelf water transport on nutrients and phytoplankton in the East China Sea: A model study.
Ocean Science, 7(1), 27–43. https://doi.org/10.5194/os-7-27-2011
Zhao, L., Wei, H., & Feng, S.-Z. (2002). Annual cycle and budgets of nutrients in the Bohai sea. Journal of Ocean University of Qingdao, 1(1),29–37. https://doi.org/10.1007/s11802-002-0027-3
Zhao, T.-L., Gong, S.-L., Zhang, X.-Y., & McKendry, I. G. (2003). Modeled size-segregated wet and dry deposition budgets of soil dust aerosol
during ACE-Asia 2001: Implications for trans-Paciﬁc transport. Journal of Geophysical Research, 108, 8665. https://doi.org/10.1029/
2002JD003363

CHU ET AL.

16