Biogeosciences, 15, 749–765, 2018https://doi.org/10.5194/bg-15-749-2018© Author(s) 2018. This work is distributed under
the Creative Commons Attribution 3.0 License.

Phytoplankton growth response to Asian dust addition in thenorthwest Pacific Ocean versus the Yellow Sea
Chao Zhang1 , Huiwang Gao1,2 , Xiaohong Yao1 , Zongbo Shi3 , Jinhui Shi1 , Yang Yu1 , Ling Meng1 , and Xinyu Guo4
1 Key Laboratory of Marine Environment and Ecology, Ministry of Education of China, Ocean University of China,

Qingdao, China
2 Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science andTechnology, Qingdao 266071, China
3 School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK
4 Center for Marine Environmental Studies, Ehime University, Matsuyama, Japan
Correspondence: Huiwang Gao (hwgao@ouc.edu.cn)
Received: 5 May 2017 – Discussion started: 30 June 2017
Revised: 26 December 2017 – Accepted: 5 January 2018 – Published: 7 February 2018

Abstract. In this study, five on-board microcosm experiments were performed in the subtropical gyre, the Kuroshio
Extension region of the northwest Pacific Ocean (NWPO),
and the Yellow Sea (YS) in order to investigate phytoplankton growth following the addition of artificially modified
mineral dust (AM dust) and various nutrients (nitrogen (N),phosphorus (P), iron (Fe), N + P, and N + P + Fe). The two
experiments carried out with AM-dust addition in the subtropical gyre showed a maximum chlorophyll a (Chl a) concentration increase of 1.7- and 2.8-fold, while the cell abundance of large-sized phytoplankton (> 5 µm) showed a 1.8and 3.9-fold increase, respectively, relative to the controls.
However, in the Kuroshio Extension region and the YS, theincreases in maximum Chl a and cell abundance of largesized phytoplankton following AM-dust addition were at
most 1.3-fold and 1.7-fold larger than those in the controls,
respectively. A net conversion efficiency index (NCEI) newly
proposed in this study, size-fractionated Chl a, and the abundance of large-sized phytoplankton were analysed to determine which nutrients contribute to supporting phytoplankton
growth. Our results demonstrate that a combination of nutrients, N–P or N + P + Fe, is responsible for phytoplankton
growth in the subtropical gyre following AM-dust addition.
Single nutrient addition, i.e., N in the Kuroshio Extension region and P or N in the YS, controls the phytoplankton growthfollowing AM-dust addition. In the AM-dust-addition experiments, in which the increased N–P or P was identified todetermine phytoplankton growth, the dissolved inorganic P

from AM dust (8.6 nmol L−1 ) was much lower than the theoretically estimated minimum P demand (∼ 20 nmol L−1 ) for
phytoplankton growth. These observations suggest that additional supply augments the bioavailable P stock in incubatedseawater with AM-dust addition, most likely due to an enhanced solubility of P from AM dust or the remineralizationof the dissolved organic P.

1

Introduction

Aeolian dust deposition can supply bioavailable nutrientssuch as nitrogen (N), phosphorus (P), and iron (Fe) to theupper ocean layers (Duce et al., 1991; Jickells et al., 2005;
Kanakidou et al., 2012). Observational and modelling studies have demonstrated that external nutrient input can stimulate primary productivity, strengthen nitrogen fixation, alter phytoplankton size, and potentially enhance carbon sequestration by the biological pump in the ocean (Mills etal., 2004; Maranon et al., 2010; Liu et al., 2013). A wellrecognized aspect of dust deposition is the iron fertilization effect in high-nutrient low-chlorophyll (HNLC) regions(Martin, 1991; Boyd et al., 2007). Recently, many studies have attempted to explore the primary chemicals that
promote phytoplankton growth following dust deposition in
low-nutrient low-chlorophyll (LNLC) regions, which cover∼ 60 % of the ocean area worldwide (Moore et al., 2008;
C. Guo et al., 2012; Ridame et al., 2014; Li et al., 2015).

Published by Copernicus Publications on behalf of the European Geosciences Union.

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C. Zhang et al.: Phytoplankton growth response to Asian dust addition

For example, dissolved Fe and P from deposited dust werereported to stimulate nitrogen fixation in the oligotrophic region of the eastern tropical North Atlantic Ocean (Mills etal., 2004). In the oligotrophic region of the western North
Atlantic Ocean off Barbados, a greater concentration of dissolved N and Fe relative to P, arising from the deposited dust,
likely favoured the growth of Prochlorococcus, but limited
the activity of diazotrophs (Chien et al., 2016). Moreover, thereported positive effect of dust deposition on primary production in the central Atlantic Ocean decreased with increasing
oligotrophy of the seawater (Maranon et al., 2010). However,studies in areas other than the North Atlantic Ocean and theMediterranean Sea are scarce.
Dust particles frequently mix with anthropogenic aerosolson their transport pathway to the oceans (Guieu et al., 2010;
Shi et al., 2012; Herut et al., 2016). The response of phytoplankton to the added dust particles mixed with anthropogenic aerosols appeared to be more sensitive in oligotrophic waters than in moderately nutrient-enriched waters(C. Guo et al., 2012). Unlike in HNLC and LNLC regionsof the oceans, the response of phytoplankton to dust deposition in coastal seas that receive a relatively large quantityof nutrients from rivers is poorly understood. A few studies
showed that dissolved N from the added dust likely stimulated phytoplankton growth in the Yellow Sea (YS; Liu etal., 2013). Added Fe instead of other dissolved nutrients fromatmospheric deposition played an important role in stimulating phytoplankton growth in the East China Sea (Meng etal., 2016). The complex responses of phytoplankton growthto dust deposition are worthy of investigation.
The N : P ratio of dust deposition is much higher than the
Redfield ratio (N : P = 16; Baker et al., 2003; C. Guo et al.,2012), which reflects the average cellular N : P stoichiometry
for oceanic phytoplankton (Arrigo, 2005). Although the deposited P was deficient relative to the demands of the resident
phytoplankton in the ocean surface, a few studies showed thatthe input of dust could compensate for P deficiency to someextent by stimulating the biogenic conversion of dissolved
organic P (DOP) to dissolved inorganic P (DIP) or a slow release of DIP from dust (Ridame and Guieu, 2002; Mackey
et al., 2012; Krom et al., 2016). This supply of bioavailable
P seemingly varies substantially across different oceanic regions and is affected by many factors, including dust sources
and its mixing with anthropogenic pollutants, P demand, andthe uptake of nutrients that are co-limiting for phytoplankton in the seawater (Mackey et al., 2012). It remains a challenge to accurately estimate the supply of bioavailable P for
phytoplankton growth induced by dust deposition in specificenvironments.
The arid regions of eastern Asia are the most importantmineral dust source to the western Pacific Ocean (Shao etal., 2011). In spring, strong westerly winds can carry large
amounts of mineral dust from the Asian continent along acorridor between 25 and 45◦ N and bring significant amountsof nutrients to downwind areas, including the coastal seas of
Biogeosciences, 15, 749–765, 2018

China and Japan and the northwest Pacific Ocean (NWPO;
Shao et al., 2011). During this long-range transport, the contents of bioavailable nutrients in the Asian dust might increase through mixing with air pollutants such as sulfur dioxide and nitrogen oxides (Formenti et al., 2011). The subtropi−
cal gyre in the NWPO is an LNLC region with NO−
3 + NO2
3−
and PO4 concentrations generally maintained at nanomolar levels (Hashihama et al., 2009). Seawater in the Kuroshio
Extension region, however, shows flexible characteristics innutrients, which is ascribed to the confluence of the Oyashio
current with replete nutrient stocks and that of the Kuroshio
current with impoverished nutrient stocks (Measures et al.,2006; Kitajima et al., 2009). On the other hand, the YS is asemi-enclosed continental shelf region, which is located on
the margin of the NWPO surrounded by the Chinese mainland and the Korean Peninsula. Seawater in the YS exhibitshigh nutrient levels but varying nutrient-limiting conditions,for example N or P limitation (Liu et al., 2003). Thus, the
NWPO and YS are the ideal zones to explore how Asian dust
deposition influences phytoplankton growth and community
size shifts under varying nutrient levels in seawaters.
In this study, we conducted on-board bioassay incubations
using artificially modified mineral dust (AM dust) collectedfrom the Gobi Desert of China and native phytoplankton assemblages collected from the NWPO and YS to investigate
the effect of atmospheric nutrients and trace metal inputs
on phytoplankton growth. The measured concentrations of
Chl a in the nutrient treatments (i.e., N, P, Fe, N + P, andN + P + Fe additions) against the control were used to determine the nutrient limitation in the subtropical gyre, theKuroshio Extension region of the NWPO, and the YS, respectively. The concentrations of total and size-fractionatedChl a and the abundances and community structures of largesized phytoplankton (> 5 µm) were determined to study the
responses of different-sized phytoplankton to the nutrients
supplied by AM dust. A net conversion efficiency index(NCEI) is proposed to identify the key nutrient(s) in determining the increase in Chl a concentrations following AMdust addition at different incubation stations. Finally, we
analysed the minimum P consumption that supports phytoplankton growth following AM-dust addition to estimate the
P budget of the added dust.

2
2.1

Materials and methods
Preparation of AM dust

We collected surface soil samples (42.37◦ N, 112.97◦ E) fromthe Gobi Desert, one of the most important sources of dust
events crossing over the YS and NWPO (Ooki and Uematsu,
2005; Shao et al., 2011). The soil samples were crushed,sieved to less than 20 µm particle size, and freeze-dried (Shiet al., 2009). To account for the ageing of dust particles in
the atmosphere, we followed Guieu et al. (2010) by mixing
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C. Zhang et al.: Phytoplankton growth response to Asian dust addition

751

Table 1. Experimental information and baseline conditions at the sampling stations.

Sampling date
Incubation time
Sampling location
Sea surface temperature(SST, ◦ C)
Mixed layer depth(MLD, m)Chl a (µg L−1 )−−1NO−
3 + NO2 (µmol L )3−
PO4 (µmol L−1 )N : P (µmol : µmol)
Micro-sized Chl a (%)
Nano-sized Chl a (%)
Pico-sized Chl a (%)
Large-sized phytoplankton
abundance (cell mL−1 )Diatoms (cell mL−1 )Dinoflagellates (cell mL−1 )

Ar4 (S1)(G7) S2K4 (S3)B7 (S4)

H10 (S5)2014.3.23
10 days29.5◦ N, 142.5◦ E
18.9

2014.4.5
9 days30.0◦ N, 148.5◦ E
18.3

2014.4.14
9 days34.0◦ N, 144.0◦ E
18.6

2014.5.9
10 days37.0◦ N, 123.2◦ E
9.8

2014.4.29
9 days35.0◦ N, 124.0◦ E
12.6

150

82

103

–

18

0.24
0.26
0.05
5
6
18
76
17

0.50
0.04
0.05
<1
8
19
73
10

1.28
0.51
0.10
5
28
23
49
79

1.58
3.20
0.10
32
14
36
50
35

2.74
0.28
0.04
7
27
37
36
314

12
5

6
4

74
5

16
19

286
28

the soil with synthetic cloud water in a cleaned polypropylene bottle, then spread the solution on a polystyrene tray andevaporated the aqueous phase under clean air flow in a fume
hood. A more detailed modification protocol is presented in
the Supplement (Text S1 and Table S1). These treated soil
dust particles are referred to as “AM dust”. Clean plastic orplastic-coated materials were used for the preparation of AM
dust to avoid metal contamination.
2.2

Experimental design

Five AM-dust-addition bioassay experiments were carriedout on-board the R/V Dongfanghong II during two cruises
in 2014 at stations Ar4, G7, and K4 in the NWPO (Cruise I:
March–April) and B7 and H10 in the YS (Cruise II: April–
May; Fig. 1 and Table 1). Based on the baseline Chl aconcentrations (Table 1), the five stations were redefined as
S1 (Ar4), S2 (G7), S3 (K4), S4 (B7), and S5 (H10) in ascending order. Surface seawater (2–5 m) was collected using
acid-washed Teflon-coated Go-Flo bottles mounted on a SeaBird CTD assembly (SBE 911, USA) and filtered througha 200 µm acid-washed mesh to remove larger grazers. Filtered seawater with different additions (true replicates, detailed in Table 2) was randomly dispensed into 18 pre-acidwashed and sample-rinsed (three times) Nalgene polycarbonate bottles (20 L each). Water samples in the incubated bottles were collected before the additions to characterize thebaseline seawater samples and immediately after the additions to characterize the amended seawater (day 0). Surface
seawater was pumped into the microcosm equipment, i.e.,
three large plastic vessels, to stabilize the temperature of the
incubation systems (Liu et al., 2013). The incubation experwww.biogeosciences.net/15/749/2018/

iments were processed over 9–10 days under natural light.
Water samples were collected from incubated bottles at 08:00
every day except day 1 (i.e., day 2 through day 9–10) to determine Chl a and nutrient concentrations and on certain days
for phytoplankton identification and enumeration.
Treatments included AM-dust and single nutrient (N, P,
or Fe) additions as well as N + P and N + P + Fe (Table 2).
Previous studies showed that the annual deposition flux ofAsian dust in the YS and NWPO regions ranged from 10 to
80 g m−2 yr−1 (Gao et al., 1992; Brown et al., 2005). An extreme dust storm event accompanied by wet precipitation in
the YS can lead to a considerable dust deposition flux in thisrange (Shi et al., 2012). Considering these results, we added
2 mg L−1 of the AM dust to the incubated seawater to simulate deposition due to a strong dust event (20 g m−2 ) in theupper 10 m water layer in the YS (Liu et al., 2013). We added
the same amount of AM dust for incubation experiments in
the NWPO for comparison. This amount of added dust has
been widely used in other studies as well (Mills et al., 2004;
Maranon et al., 2010). Based on the N-deposition flux in the
NWPO (Kim et al., 2014) and an estimate of the N addition
by a dust event in the surface water of the YS (Shi et al.,2012), we added 40 µmol NaNO3 into the 20 L bottles for the
N-related treatments (N, N + P, and N + P + Fe additions) toincrease the N concentration by 2 µmol L−1 . The added P
and Fe amounts in the incubation systems were 0.2 µmol L−1
and 2 nmol L−1 , respectively, based on the nutrient-addition
experiments conducted in the NWPO and YS (Noiri et al.,2005; Liu et al., 2013; Table 2).
One-way analysis of variance (ANOVA) was used to assess significant differences in the mean values of the selectedparameters among various treatments, and then Dunnett’s

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C. Zhang et al.: Phytoplankton growth response to Asian dust addition

Table 2. Treatments to the bioassay incubation experiments.
Incubation no.

Treatments

Amended concentrations

1
2
3
4
5∗
6
7

Control
AM dustNaNO3
NaH2 PO4
FeCl3
NaNO3 + NaH2 PO4
NaNO3 +NaH2 PO4 +FeCl3–
2 mg L−1
2 µmol L−1
0.2 µmol L−1
2 nmol L−1
2 µmol L−1 + 0.2 µmol L−1
2 µmol L−1 + 0.2 µmol L−1 + 2 nmol L−1∗ Only at stations S2 and S4.

Figure 1. Locations of the five seawater collection stations for the microcosm experiments (the base map reflects an average composite of
Chl a concentrations in March–May 2014 obtained from the NASA website at https://modis.gsfc.nasa.gov/data/dataprod/chlor_a.php).

test was used to compare these treatments with the control
using SPSS (Statistical Product and Service Solutions) software.
2.3

Chl a concentration

From each bottle, a 300 mL seawater sample was sequentially filtered through 20, 2, and 0.2 µm Whatman polycarbonate filters to determine size-fractionated Chl a concentrations, i.e., pico-sized (0.2–2 µm), nano-sized (2–20 µm),
and micro-sized (> 20 µm) Chl a. The pigments on the filters
were extracted in 90 % acetone at −20 ◦ C over 24 h in thedark and measured on a Turner Designs Trilogy fluorometer(Strickland and Parsons, 1972). The total Chl a concentration was calculated as the sum of the three size-fractionatedvalues.

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2.4

Inorganic nutrients and trace metals−+
To determine the soluble nutrients such as NO−
3 , NO2 , NH4 ,3−
and PO4 leached from AM dust, oligotrophic seawater was
pre-filtered by 0.2 µm glass fibre filters and used for extracting these ions at ∼ 0◦ for 30 min in an ultrasonic bathfilled with ice and water. A 200 mL seawater sample retrieved
from each of the incubation bottles was filtered through preacid-washed cellulose acetate membranes and filtrates werestored immediately at −20 ◦ C in acid-washed high-density
polyethylene bottles for nutrient analysis in the laboratory.
Soluble nutrients leached from AM dust and in the incubated seawaters were measured following the automated colorimetric technique described by Grasshoff et al. (1999)
and Ridame et al. (2014) using a QuAAtro continuous-flow
analyser (SEAL Analytical). Detection limits of this instrument were defined as 3 times the standard deviation of thewww.biogeosciences.net/15/749/2018/

C. Zhang et al.: Phytoplankton growth response to Asian dust addition
blank, which corresponds to 30, 7, 80, and 40 nM for NO−
3,
+
3−
+
NO−
,
NH
,
and
PO
,
respectively.
Note
that
the
NH
con2
4
4
4
centrations were determined only for the leached solutionof AM dust. We followed the method proposed by Hsu etal. (2010) to determine the concentrations of soluble trace
metals leached from AM dust using an ICP-MS. The recovery yield, accuracy, and detection limit are summarized inTable S2.
2.5

Phytoplankton identification and enumeration

Seawater samples (300 mL volume) were collected from thebaseline seawaters at each station and incubated bottles on
day 4 from S1 and S2, day 3 from S3 and S5, and day 5 from
S4 for the identification and enumeration of large-sized phytoplankton (> 5 µm). The sampling dates selected during the
incubation experiment were either close to or corresponded
exactly with the days that showed the maximum Chl a concentrations (Fig. S1). The sampled seawater was fixed with
1 % Lugol’s iodine and stored in the dark until microscopic
observation in the laboratory (Burson et al., 2016). Before
analysis, the preserved samples were settled for 48 h in thedark and then concentrated to 10 mL volume in glass cylinders. Large-sized phytoplankton were identified and enumerated using a Nikon ECLIPSE TE2000-U inverted microscope. To illustrate the responses of different phytoplankton
to various additions, the detected phytoplankton species weredivided into two major functional groups: diatoms and dinoflagellates. The dominant species of diatoms found in thisstudy were Nitzschia spp., Chaetoceros spp., Thalassiosira
spp., Skeletonema spp., Cylindrotheca closterium, and Rhizosolenia setigera.
2.6

Protocol of data analysis

calculated using the following equation:t
P

NCEI =

www.biogeosciences.net/15/749/2018/(Chl aTi − Chl aCi )

i=0

1N

,

(1)

where Chl aTi and Chl aCi represent the Chl a concentrations on the ith day, i.e., day 0, day 2, or day 3–5, in thetreatments and the control (µg L−1 ), respectively; 1N is thedecreased N concentration in the treatment minus that in thecontrol during the successive increase in the incubation period (µmol L−1 ). The decreased N concentration equals the−difference in NO−
3 + NO2 before and after the initial increase period. A large NCEI value represents a positive effect of the added N on phytoplankton growth, and a value
close to zero represents no effect. The larger the NCEI value,
the higher the N-utilization efficiency by the phytoplankton.
Theoretically, the maximum increase in Chl a concentration
can also be used to calculate NCEI. Considering the accumulation and degradation of Chl a, the real net conversion efficiency should be among the NCEI values between the two
approaches.
We also defined the consumed ratio of N : P (hereafter,
CN : P ) and supply ratio of N : P (hereafter, SN : P ) to illustrate
the changing stocks of bioavailable N and P in various incubation experiments. CN : P was the ratio of the difference−in NO−
3 + NO2 concentrations at the beginning and the endof the successive increase in the incubation period to that of
−
−
3−
PO3−
4 ; SN : P was the amended ratio of NO3 + NO2 to PO4
concentrations in the incubated seawaters on day 0 in various
treatments.
3
3.1

In this study, Chl a concentrations generally showed a bellshaped growth curve at all stations with the maximum concentration occurring at around 2–5 days (Fig. S1). We focused on analysing the initial 2–5 days when Chl a concentration shows a steady increase during the incubation period.
For example, it took 5 days to reach the maximum value of
Chl a in the AM-dust treatment and the control at S1. In othertreatments at S1, 3 or 4 days were required to reach the maximum value. Thus, we define the initial 5 days as a successive
increase in Chl a concentration at S1. The same definition is
also applicable for other stations. The duration of 2–5 days
for incubation has been widely used in other microcosm experiments (Herut et al., 2005; Tanaka et al., 2011; C. Guo etal., 2012; Li et al., 2015) and is expected to minimize the effects of bottle enclosure and possible deviation from the natural environment (Mackey et al., 2012; Coelho et al., 2013).
A net conversion efficiency index (NCEI) was introduced
to quantify the differences in N-utilization efficiency among
the AM-dust treatments and N, N + P, and N + P + Fe treatments. NCEI (unit: µg L−1 / µmol L−1 , i.e., g mol−1 ) was

753

Results
Characteristics of baseline surface seawaterand AM dust

Stations S1, S2, and S3 are in the open ocean and were characterized by warm surface seawaters with sea surface temperature (SST) larger than 18◦ and a deep mixed layer witha depth larger than 80 m. Stations S4 and S5 are in the YS
and the SST and MLD therein were less than 13◦ and 20 m,
respectively (Table 1). The winter cooling induces a lower
water temperature in the shallow YS than in the deep open
ocean. Therefore, the short warming time before our observations during the springtime cannot reverse this situation.
The weaker winds and lesser loss of heat flux over the landsurrounding YS than over the open ocean lead to a shallower
mixed depth at S4 and S5 than at S1–S3.
Low concentrations of Chl a (≤ 0.50 µg L−1 ) and nutrients
−
−1
−1
(NO−
PO3−
3 + NO2 ≤ 0.26 µmol L ,4 = 0.05 µmol L )were observed at S1 and S2 in the subtropical gyre of the
NWPO (Table 1), indicating oligotrophy (Hashihama et al.,2009). At S3 in the Kuroshio Extension and S4 in the YS,
Chl a and nutrient concentrations were at least 2-fold higher
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C. Zhang et al.: Phytoplankton growth response to Asian dust addition

Table 3. Nutrient and soluble trace metal contents in artificially modified and untreated dust and the theoretically increased corresponding
concentrations in the incubated seawaters amended with AM dust.
Nutrients (µmol g−1 )AM dust
Untreated dust
Increased concentrations
amended with AM dust
(nmol L−1 )b

Soluble trace metals (µg g−1 )

NO−
3

NO−
2

NH+
4

PO3−
4

Fe

Mn

Cu

Cd

Pb

Co

Zn

532.9
133.2
1066

34.2
8.6
68.4

10.3
10.5
20.6

4.3
1.3
8.6

473.1
22.7
16.90

413.5
1.66
15.05

0.23
NDa
7.2 × 10−3

0.04
ND
7.1 × 10−4

0.24
ND
2.3 × 10−3

2.58
ND
0.09

4.27
0.03
0.13

a “ND” means no detection. b Calculated by dividing the added amounts of nutrient and soluble trace metals with AM-dust input by the incubation volume of 20 L.

than those at S1 and S2, indicating an increased trophic state
at S3 and S4. Although the nutrient levels at S5 in the YS
were comparable to those at S1, the Chl a concentration of
2.74 µg L−1 was close to the values during spring blooms in
the YS (Liu et al., 2003; Fu et al., 2009; Liu et al., 2013).
The N : P ratios at S1, S2, S3, and S5 were far lower thanthe Redfield ratio (16 : 1), while that at S4 was as high as
32 (Table 1). Pico-sized Chl a accounted for > 70 % of thetotal Chl a at S1 and S2, but it decreased to less than ∼ 50 %at S3, S4, and S5. Specifically, large-sized phytoplankton
abundance showed an increasing trend from < 20 cells mL−1
at S1 and S2 to 35 cells mL−1 at S4 and 79 cells mL−1 at
S3, to the highest value of 314 cells mL−1 at S5. Diatoms
dominated the large-sized phytoplankton community at S1,
S3, and S5, and a co-dominance of dinoflagellates was noted
at S2 and S4 (Table 1).
The concentration of dissolved inorganic nitrogen (DIN,−+−1i.e., NO−
3 + NO2 + NH4 ) in the AM dust was 577 µmol g(Table 3) and increased by a factor of 4 against that in
the untreated dust. A notable increase in the PO3−
4 content (4.3 µmol g−1 ) in the AM dust was observed relative tothe untreated dust (1.3 µmol g−1 ). The abundances of DIN,
PO3−
4 , and soluble Fe in the AM dust were generally consistent with the values observed in a strong dust event that
occurred over the YS in the spring of 2007 (Shi et al., 2012).
The N : P ratio of ∼ 134 in the AM dust was far greaterthan 16 (Redfield ratio) and similar to those in Asian dust
aerosols previously reported (Shi et al., 2012; Liu et al.,−2013; Chien et al., 2016). The NO−
3 + NO2 concentrationin the incubated seawater after AM-dust addition increased
up to ∼ 1.13 µmol L−1 (Table 3 and Fig. 2), which is larger−
than the baseline NO−
3 + NO2 stocks at S1, S2, S3, and S5,
but accounted only for approximately one-third of the baseline stock at S4 (Table 1). However, the increase in PO3−
4(∼ 8.6 nmol L−1 ) following AM-dust additions was negligible compared with the baseline P stock at each station (Tables 1 and 3).

Biogeosciences, 15, 749–765, 2018

3.2

Variation in nutrient and total Chl aconcentrations during incubation experiments

During the successive increase in the incubation period (ini−tial 2–5 days of the incubations; Sect. 2.6), NO−
3 + NO2 andPO3−4 concentrations generally showed a decline in the control and all treatments (Fig. 2). At each station, the most−3−
obvious decline in NO−
3 + NO2 and PO4 concentrations
in various treatments occurred when N + P or N + P + Fe
was added. The net declines were 1.49–4.66 µmol L−1 for−−1 for PO3− . The deNO−
3 + NO2 and 0.18–0.27 µmol L
4−−1cline was 0.49–2.99 µmol L for NO−
3 + NO2 and 0.10–
0.27 µmol L−1 for PO3−
4 followed by N and P additions, respectively. For P addition alone at S4, the decline in PO3−
4
was comparable to those in combined nutrient additions−−1(0.27 µmol L−1 ) and that of NO−
3 + NO2 (2.99 µmol L )was 1.3-fold larger relative to the control. Correspondingly,
the addition of N + P + Fe induced the largest increases intotal Chl a (hereafter, Chl a) among all treatments, and theincreases were significant against the controls (p < 0.05)
at all stations (Fig. 3). The maximum concentrations of
Chl a in the N + P + Fe treatments reached 1.70 µg L−1 at
S1 (day 4), 1.65 µg L−1 at S2 (day 5), 3.50 µg L−1 at S3(day 3), 4.98 µg L−1 at S4 (day 4), and 5.08 µg L−1 at S5(day 2). This was a 1.9- to 7.1-fold increase compared tothe baseline and was 1.5- to 3.0-fold larger than the controls
in the five incubation experiments. The time series of Chl ain N + P and N + P + Fe treatments almost overlapped at all
stations except S2, where the maximum value of Chl a in
the N + P treatment (1.15 µg L−1 ) was only 70 % of that in
the N + P + Fe treatment. Significant increases in Chl a relative to the control were also observed in N treatments at S1,
S2, S3, and S5 and in P treatments at S2 and S4 (p < 0.05).
The maximum concentrations of Chl a in the N treatments
at S1 (0.73 µg L−1 on day 3), S2 (0.67 µg L−1 on day 2),S3 (2.14 µg L−1 on day 3), and S5 (4.34 µg L−1 on day 2)
and in the P treatments at S2 (0.79 µg L−1 on day 2) and S4(4.46 µg L−1 on day 3) showed a 1.3- to 3.1-fold increase
compared to the baseline and were 1.2- to 1.6-fold larger
than the controls. There was no significant increase in Chl a
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C. Zhang et al.: Phytoplankton growth response to Asian dust addition

755

−
3−
Figure 2. Changes in NO−
3 +NO2 and PO4 concentrations during the successive increase in the incubation period at each station. Shaded
areas indicate the values below the detection limit.

relative to the control in the rest of the additions at the fivestations.
−
Following the addition of AM dust, NO−
3 + NO2 con−1
centrations declined by 1.06 µmol L at S1, 0.88 µmol L−1
at S2, 1.36 µmol L−1 at S3, 2.93 µmol L−1 at S4, and0.36 µmol L−1 at S5. The declines were generally larger thanthe values in the baseline (Fig. 2). PO3−
concentrations
4in AM-dust treatments declined by 0.04–0.11 µmol L−1 andwere similar to those of the control during the successive increase in the incubation period at each station. Correspondingly, the maximum concentration of Chl a following AMdust addition was 1.04 µg L−1 at S1 (day 5), 1.54 µg L−1 at
S2 (day 5), 2.23 µg L−1 at S3 (day 2), 3.27 µg L−1 at S4(day 5), and 3.13 µg L−1 at S5 (day 2; Fig. 3), which was
1.1- to 4.4-fold larger against the baseline. The increases in
Chl a were significantly different (p < 0.05) from the control
at S1, S2, S3, and S5. The maximum Chl a concentration following AM-dust addition was 1.7-fold, 2.8-fold, and 1.3-foldlarger than those in the controls at S1, S2, and S3, respectively. At S4 and S5, the maximum Chl a concentration in
the AM-dust treatments was comparable to those in the controls. However, the Chl a concentrations remained relatively
high in the AM-dust treatments, while showing a decreasing
trend in the controls (Fig. 3).

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3.3

Variation in the size-fractionated Chl aconcentrations during incubation experiments

When the size-fractionated Chl a was examined in various
treatments at the five stations, a few notable changes wereobserved, as highlighted below.
a. In the controls, the dominant contributors to the total
Chl a were pico-sized cells at S1, S2, and S4 and nanosized cells at S5, while they changed from pico-sized tomicro-sized cells at S3 during the successive increasein the incubation period (Fig. 4). The addition of AM
dust increased the Chl a concentrations of all sizes andthe dominant contributor was consistent with those in
the controls at the five stations. However, the magnitude of Chl a increase was the highest for micro- or
nano-sized cells following AM-dust additions. For example, the largest increase in maximum Chl a occurredin micro-sized cells at S1 (2.0-fold), S2 (4.4-fold), S4(1.4-fold), and S5 (1.6-fold) and in nano-sized cells at
S3 (1–3 fold) compared with the controls.
b. Size-fractionated Chl a in N + P and N + P + Fe additions showed the largest and most similar increases at
S1, S3, S4, and S5, especially in the micro-sized range,in which the maximum Chl a concentrations showed a
1.2- to 6.5-fold increase against the controls (Fig. 4).
For station S2, the micro- and nano- sized Chl a showed
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Figure 3. Changes in Chl a during the successive increase in the incubation period at each station.

higher increases in N + P + Fe treatments than in N + P
treatments, whereas the opposite was true for the picosized Chl a. The addition of N or P alone also led to
an increase in size-fractionated Chl a to some extent
at all stations. The size-fractionated Chl a in N treatments at S1, S3, and S5 increased noticeably; for example, the maximum Chl a showed the largest increase innano-sized cells by a factor of 1.6 at S1 and 1.4 at S3
and in micro-sized cells by a factor of 2.2 at S5 relative to the controls. A clear increase was also observedin the P treatment at S2 and S4; for example, the maximum Chl a concentrations showed a 1.8-fold (nano) and
1.5-fold (micro) increase against the controls (Fig. 4).
There was no noticeable increase in any of the sizefractionated Chl a following Fe addition at S2 and S4.
c. The results of size-fractionated Chl a demonstrated
that the micro- and nano-sized phytoplankton generally
showed a stronger response than pico-sized cells following AM-dust and various nutrient additions, although
the extent of increase varied among the stations.
3.4

Variation in large-sized phytoplankton abundanceand community during incubation experiments

After 2–5 incubation days, diatoms generally dominated thelarge-sized phytoplankton community in all treatments at thefive stations. Chaetoceros spp. and Nitzschia spp. comprised
the largest fraction of diatoms in all treatments at S1, S2, andS3. For stations S4 and S5, the dominant species of diatoms
did not change compared with those in the baseline seawaters (Fig. 5). Specifically, the cell abundance of large-sized
phytoplankton in the controls increased to 37 cells mL−1 at
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Figure 4. Changes in size-fractionated Chl a during the successive
increase in the incubation period at each station.

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Figure 5. Changes in the taxonomic structure of a large-sized phytoplankton community before (i.e., baseline) and during (i.e., control
and various treatments) the successive increase in the incubation period at each station. (a) Cell abundance of large-sized phytoplankton.
(b) Relative abundance; i.e., the contribution of specific species to the large-sized phytoplankton community in cell abundance.

S1, 39 cells mL−1 at S2, 422 cells mL−1 at S3, 93 cells mL−1
at S4, and 643 cells mL−1 at S5. Similar to the response of
Chl a, additions of N + P and N + P + Fe increased the phytoplankton abundances noticeably in all treatments by about
2.5- to 2.7-fold at S1 and S5, 3.1- to 3.3-fold at S3, and 2.7fold at S4 relative to the controls. For single nutrient treatments, N additions at S1, S3, and S5 and P additions at S4 induced the highest increases in cell abundance, with 1.5-, 1.6-,
2.3-, and 1.9-fold higher values, respectively, than those in
the controls. The cell abundance of large-sized phytoplankton in AM-dust treatments relative to the controls increasedby 1.8-fold at S1 and 1.7-fold at S3 and S5, but showed anegligible increase at S4. Moreover, the increases following AM-dust additions were comparable to and sometimes
even larger than those in the N treatments at S1, S3, andS4, but lower than the latter at S5. At S2, the cell abundancewith AM-dust addition increased by 3.9-fold against the controls, which was comparable to those in the N + P treatments(Fig. 5).

4
4.1

Discussion
Nutrient limitation in the NWPO and YS

Building on the results mentioned above (Fig. 3 and Table 1), we summarized the nutrient-limiting status at the fivestations. At S1, phytoplankton growth was very likely colimited by N and P because (1) N addition induced a significant increase in Chl a against the controls (p < 0.05),(2) there were significant increases in Chl a following N + P
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additions compared with the N treatments (p < 0.05), and(3) there were no significant differences in Chl a between
N + P and N + P + Fe treatments (p > 0.05). At S2, a significant increase in Chl a was observed in the P, N + P,
and N + P + Fe treatments (p < 0.05) against the controls,
and the addition of N + P and N + P + Fe induced a significantly larger response relative to the P treatments (p < 0.05).
Chl a concentrations in the N + P + Fe treatments were significantly larger than in the N + P treatments on days 4–
5. Therefore, we concluded that phytoplankton at S2 wereprimarily co-limited by N, P, and Fe (Fig. 3). At S3, N
addition induced a significant increase in Chl a comparedwith the controls, while an even larger significant increase
was observed upon N + P (+Fe) addition relative to the N
treatments. Thus, phytoplankton were primarily co-limited−3−
by N and P at S3. Accordingly, NO−
3 +NO2 and PO4
concentrations in N + P (+Fe) treatments at the three stations decreased by 73–100 %, which is larger than the de−cline in NO−
3 +NO2 concentrations after adding N alone andPO3−
4 concentrations after adding P alone (43–70 %; Fig. 2).
Such co-limiting conditions have been widely reported in theoceans, especially in oligotrophic regions such as the eastern Mediterranean Sea (Tanaka et al., 2011) and the South
China Sea (C. Guo et al., 2012). Moore et al. (2013) argued
that low abundances of N and P in oligotrophic environments are likely to simultaneously reach the limiting levels
for phytoplankton growth. Note that phytoplankton at S3 inthe Kuroshio Extension showed a greater response to N thanP addition. The intrusion of Kuroshio–Oyashio transition water from the north and Kuroshio water from the southwest,

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both carrying macronutrients typically with N : P < 16, likely
changed the nutrient stocks of the seawaters at S3 (Whitney,
2011; X. Guo et al., 2012; Yatsu et al., 2013). A low primary productivity in the Kuroshio Extension region during
the springtime was also indicated by the low availability ofnitrate in the seawater (Nishibe et al., 2015).
Similarly, we also found that P and N were the primary
limiting nutrients at S4 and S5, respectively (Fig. 3). This isconsistent with the baseline N : P ratios at S4 (> 16) and S5(< 16; Table 1). In fact, the PO3−
4 after adding P alone at S4−and NO−
3 + NO2 after adding N alone at S5 decreased by
80 and 100 %, respectively, during the successive increase in
the incubation period (Fig. 2). Complex hydrographic conditions, for example various riverine inputs and atmosphericdeposition, create a large spatio-temporal variation in nutrient concentrations in the YS (Liu et al., 2003). The riverine
input and atmospheric deposition with a high N : P (> 16)
lead to relatively P-deficient conditions, while the rapid uptake by phytoplankton characterized by a lower N : P (< 16)during the bloom period likely accelerates the decline of
P concentrations in the surface seawaters (Liu et al., 2003,
2013; Arrigo, 2005). In general, the N : P ratios during thespringtime in the coastal waters (near S4) are higher than 16
and lower than 16 in the central waters (near S5) of the YS(Fu et al., 2009). The primary P- or N-limiting conditionsin the surface seawaters of the YS have also been widelyreported in previous studies (Wang et al., 2003; Liu et al.,2013).
4.2

Positive effects of AM dust on phytoplankton
growth in the NWPO and YS

It was clear from the data that AM-dust addition increased
the Chl a concentrations and large-sized phytoplankton
abundance to varying extents at the five stations (Figs. 3, 4
and 5). However, the increased concentrations of nutrients(e.g., N, P, and Fe) in AM-dust additions were different fromthose in various nutrient additions. In this study, the NCEI
was proposed to quantitatively compare the utilization of N
for the growth of phytoplankton among treatments and infer
which nutrients in the AM dust primarily supported phytoplankton growth.
−NO−
3 + NO2 was theoretically added in the AM-dust
treatments at a concentration of 1.13 µmol L−1 (Table 3).
−
However, the increase in NO−
3 + NO2 concentration was−1
only 0.59–0.85 µmol L immediately after the addition andmixing steps (i.e., on day 0) at the five stations, which was−
about 52–75 % of the added NO−
3 + NO2 . Similar trends−−
were also observed for NO3 + NO2 and PO3−
4 concentrations in the nutrient treatments (Fig. 2). The time interval ofadding materials to the incubation bottles and sampling seawater for nutrient measurement was 1–2 h. Microbial uptake
and scavenging by the cell surface and bottle wall possibly
decreased the concentrations of nutrients at 1–2 h, leading tomeasured values smaller than the theoretical values. When
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the concentrations of NO−
3 + NO2 and PO4 decreased in
the seawater, those absorbed by the cell surface and bottle
wall had the potential to be released into the solution again
to reach equilibrium (Liu et al., 2013). Thus, the theoretically
added N and P, plus the baseline concentrations in the seawaters, were considered the amended concentrations on day 0,
which were used for calculating the NCEI.
The added N in AM-dust and N-related treatments generally stimulated phytoplankton growth to varying extents,
as indicated by the large NCEI values (Fig. 6). Note that
the NCEI in N treatments (hereafter NCEIN ) at S4 wasaround 0 g mol−1 because the phytoplankton were primarily limited by P. The significant difference in NCEI among
various nutrient treatments can also reflect the roles playedby other nutrients such as P and Fe in affecting the Nutilization efficiency. The NCEI values in the N + P + Fe
treatments were 1.6 ± 0.1 g mol−1 at S1, 1.5 ± 0.1 g mol−1
at S3, 2.7 ± 0.2 g mol−1 at S4, and 1.4 ± 0.1 g mol−1 at
S5, which are comparable with those in N + P treatments(Fig. 6). This suggested that the effect of added Fe on the
N-utilization efficiency was negligible at the four stations.
Although the added Fe alone had no obvious influence on
the Chl a concentration at S2 (Fig. 3), the higher valueof NCEIN + P + Fe (1.8 ± 0.0 g mol−1 ) than the NCEIN + P(1.6 ± 0.0 g mol−1 ) therein demonstrated that Fe likely contributed to increasing the N-conversion efficiency during
Chl a generation (Twining and Baines, 2015). In addition,
the values of NCEIN + P and NCEIN + P + Fe were generally
higher than those of NCEIN at S1, S2, S3, and S4 (Fig. 6),
which is indicative of the fact that added P contributed to theincreased N-utilization efficiency at these stations. Indeed, P
is an important part of the ribosome and can promote cell division (Arrigo, 2005), which likely increased the NCEI values to some extent. Liu et al. (2013) also reported that theexcessive P relative to N (N : P < 16) in incubated seawater
could increase the biomass. There were no significant differences in the NCEI values between the various treatments
at S5, demonstrating that the effects of other nutrients (i.e.,
P and Fe) on N-conversion efficiency were negligible compared with N.
The NCEI in the AM-dust treatments was
1.3 ± 0.1 g mol−1 at S1 and 1.4 ± 0.6 g mol−1 at S4,
which was 1.7- and 16.8-fold higher than those in the
N treatments, respectively (Fig. 6). Considering the Plimiting conditions at both stations, we concluded thatthe external supply of P associated with the AM-dust
input likely also played a role in increasing the NCEI.
Moreover, the NCEIAM-dust of 2.4 ± 0.1 g mol−1 washigher than NCEIN + P + Fe (1.8 ± 0.0 g mol−1 ), NCEIN + P(1.6 ± 0.0 g mol−1 ), and NCEIN (0.3 ± 0.2 g mol−1 ) at S2.
Apart from N, P, and Fe, AM dust also provided considerable
other nutrients, for example Mn and Co (Table 3), which
may have also contributed to the phytoplankton growth in
the incubations at S2 (Coale, 1991; Jakuba et al., 2008;
Saito et al., 2008; Sunda, 2012). This potential synergisticwww.biogeosciences.net/15/749/2018/

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Figure 6. The net conversion efficiency index (NCEI) of N conversion to Chl a in AM-dust and various nutrient additions during the
successive increase in the incubation period at each station. Error
bars were calculated by propagating the standard deviation of NCEI
in various treatments; “∞” indicates that the standard deviation isat least threefold larger than the mean value of NCEI.

effect is worthy of further investigation. At S3 and S5, the
NCEI in AM-dust treatments, i.e., 1.2 ± 0.1 g mol−1 at S3
and 1.1 ± 0.5 g mol−1 at S5, were similar to those in N treatments, i.e., 1.1 ± 0.1 g mol−1 at S3 and 1.2 ± 0.2 g mol−1 at
S5 (Fig. 6), indicating a negligible effect of the dissolved P
from AM dust on NCEI.
In recent years, more studies have challenged the use of the
Redfield ratio to evaluate nutrient-limiting conditions of phytoplankton (Klausmeier et al., 2004a; Arrigo, 2005; Moore
et al., 2013). Atmospheric aerosols characterized by mineral
dust or anthropogenic pollutants contain complicated chemical components, and their deposition to oceans can leadto complicated responses of phytoplankton (C. Guo et al.,2012; Paytan et al., 2009; Meng et al., 2016). The NCEI appears to have the advantage of revealing the possible mechanisms associated with the responses to some extent. For
instance, phytoplankton at S1, S2, and S3 were under colimiting conditions of various nutrients, while the ratios of
N : P in the seawaters were lower than a Redfield ratio of
16 (indicating N limitation). The difference in NCEI values
among AM-dust and various nutrient treatments (N, P, N + P,
N + P + Fe) allows for the quantification of the role of N, P,
and Fe in stimulating phytoplankton growth (Fig. 6). Moreover, the NCEI also reveals other nutrients which may have a
promotion effect on phytoplankton at S2. Note that the calculation of NCEI was based on the change in Chl a rather thanbiomass. In general, phytoplankton biomass increased with
Chl a, which is an essential component for photosynthesis.
However, as C : Chl a ratios could vary for different phytoplankton assemblages (Sathyendranath et al., 2009), the relationship between biomass and N nutrients needs to be further
investigated.

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Figure 7. Relative change (%) in size-fractionated Chl a in AMdust and various nutrient treatments during the successive increasein the incubation period at each station. Relative change in thisstudy was calculated as 100 × ([mean in treatments − mean incontrol]/mean in control). Error bars were calculated by propagating the standard deviation of mean values in the control and various treatments; “∞” indicates that the standard deviation is at least
threefold larger than the mean value of relative change. Asterisks indicate that the treatment induces a significant difference in the meanof Chl a compared with those in the control (p < 0.05).

Figure 7 shows the changes in the three size-fractionatedChl a concentrations in the treatments relative to the corresponding controls. Generally, the relative changes in the sizefractionated Chl a in AM-dust treatments showed a decreasing trend with decreasing cell size, i.e., micro-sized ≥ nanosized ≥ pico-sized cells, which is consistent with the pattern observed in N + P + Fe treatments. Previous incubation experiments have also shown that the addition of Asian
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aerosols could shift the phytoplankton size towards larger
cells (C. Guo et al., 2012; Liu et al., 2013). Indeed, microand nano-sized cells, as indicated by faster uptake rates fornutrients and higher biomass-specific production rates, havea growth advantage relative to the pico-sized cells when theadded materials relieve the nutrient-limiting pressures (Cermeno et al., 2005; Maranon et al., 2007, 2012). The relativechanges in micro- and nano-sized Chl a in AM-dust treatments were generally higher than in the N treatments at S1,
S2, and S4. Especially for station S2, the relative changes
in micro- and nano-sized Chl a in the AM-dust treatments
were even larger than in the N + P treatments and comparable to those in the N + P + Fe treatments (Fig. 7). These
results demonstrated the importance of increased bioavailability of P at S1 and S4 and that of P and Fe at S2 following
AM-dust addition, which supported the growth of micro- andnano-sized phytoplankton.
When the cell abundances of large-sized phytoplankton
were considered, we also found that the addition of AM
dust induced larger increases than N additions after certain
incubation days at S1 and S2, as characterized by the colimitation of multiple nutrients. Especially at S2, the increasein large phytoplankton abundance was even larger than in
the N + P treatments and lower than in the N + P + Fe treatments. However, for station S3 characterized by N–P colimitation, the changes in the cell abundance of large-sized
phytoplankton in AM-dust treatments were comparable tothose in the N treatments. These results indicated that the
supply of N–P and N + P + Fe induced by AM-dust addition likely contributed to the increase in large-sized cellabundance at S1 and S2, respectively, whereas the supplied
N from AM dust likely determined the growth of largesized phytoplankton at S3 because the supply of P from theAM dust was negligible relative to the baseline P stocks(0.10 µmol L−1 ). For station S5 characterized by N limitation
alone, the addition of AM dust provided the limiting nutrient
to increase the cell abundance of large-sized phytoplankton(Fig. 5).
Diatoms generally dominated the phytoplankton community in the control and treatments during the successive increase in the incubation period at S1, S2, S3, and S5 (Fig. 5).
The addition of AM dust and limited nutrients induced anotable increase in the diatom cell abundance at the four
stations. Indeed, when the nutrient-limitation stress was relieved, diatoms tended to prosper rapidly, which was ascribedto their fast uptake rates and quick metabolic responses to enhanced nutrient availability (Fawcett and Ward, 2011; Franzet al., 2012). The dominant species of diatoms (Chaetoceros
spp., Nitzschia spp. in the open ocean and Thalassiosira
spp., Skeletonema spp., Cylindrotheca closterium, Rhizosolenia setigera, and Nitzschia spp. in the YS) in this study weresimilar to those reported in the North Pacific and YS (Noiriet al., 2005; Aizawa et al., 2005; Sun et al., 2013). Although
the dominant algae at S4 were diatoms in treatments that received various additions, a shift of community structure from
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Figure 8. The relationship between the consumed N : P ratio(CN : P ) and supply N : P ratio (SN : P ) in the control and the various
nutrient treatments during the successive increase in the incubation
period at all stations.

diatoms to dinoflagellates was observed for AM-dust andN additions relative to the control. The contributions of dinoflagellates to the large-sized phytoplankton community incell abundance reached 40–48 %, while there was only 18–
28 % among the P, N + P, and N + P + Fe treatments (Fig. 5).
This was closely related to the fast growth of diatoms as aresult of the relief from P-limiting conditions after the addition of P, N + P, and N + P + Fe. It has been reported thatdinoflagellates with lower demands and higher P-absorption
efficiency have an advantage of surviving in P-deficient conditions compared with diatoms (Egge, 1998; Zhou et al.,2008). Hence, in contrast to P-related treatments, the supplyof bioavailable P from AM dust was not enough to support
the growth of diatoms at S4 (Fig. 5).
4.3

Bioavailable P in the AM-dust-addition experiment

The increase in bioavailable P concentration following AMdust addition played an important role in stimulating phytoplankton growth at S1, S2, and S4, as mentioned above(Sect. 4.2). However, we did not detect a marked increasein the PO3−
4 concentrations in incubated seawaters following AM-dust additions during the successive increase in the
incubation period at the three stations (Fig. 2). This could
be ascribed to the gradual bioavailable P released over timeand its rapid uptake by phytoplankton with a high P demand(Mackey et al., 2012) and the easy adsorption of PO3−
4 byparticles or bottle walls (Liu et al., 2013), which likely increases PO3−
4 concentration in the incubated seawaters below the detection limit. In order to quantify the increased
bioavailable P concentrations following AM-dust addition,
we analysed the correlation of the CN : P and SN : P in AMdust and N treatments in Fig. 8.
CN : P significantly increased with SN : P (Fig. 8), and thesame trend was observed at each station (Fig. S2). Klauswww.biogeosciences.net/15/749/2018/

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761

Figure 9. Graphical presentation of consumed bioavailable P in the AM-dust treatments. SNN : P and SADN : P mean SN : P in N and AMdust treatments, respectively. CNN : P and CADN : P mean CN : P in N and AM-dust treatments, respectively. CADPmin means the minimum
consumed bioavailable P in the AM-dust treatments.

meier et al. (2004b, 2008) pointed out that the phytoplankton
in nutrient-rich environments tend to exhibit an exponential
bloomer growth with a requirement for an N : P ratio at a relatively constant value regardless of the varying nutrient supply ratios. However, when the phytoplankton tend to sustain
a competitive equilibrium status in nutrient-limited environments, for example N or P, their requirements for N : P ratios generally increase with the nutrient supply ratios. In ourstudy, the phytoplankton at the five stations were limited bydifferent nutrients and thus tended to sustain a competitive
equilibrium status. As the provided DIN following the AMdust addition was 1.15 µmol N L−1 , lower than the amount of
N when added alone (2 µmol N L−1 ), the SN : P in AM-dust
treatment was lower than that in N treatments. Thus, CN : P
in both treatments at each station would follow this pattern:
CN : P in AM-dust treatments ≤ CN : P in N treatments. The
consumed N in AM-dust treatments and N and P in N treatments can be determined on the basis of nutrient measurements at the beginning and the end of the successive increasein the incubation period (Fig. 2).
Because of CN : P in AM-dust treatments ≤ CN : P in N
treatments, an inequality can be obtained:
CADP ≥CADN × CNP
,
CNN

(2)

where CADP (CNP ) and CADN (CNN ) are the consumed−−1
bioavailable P and NO−
3 + NO2 concentrations (µmol L )in the AM-dust (N) incubation systems during the successive
increase in the incubation period, respectively. “AD” and “N”
mean AM-dust and N treatments, respectively.
The calculated result of the right term can be consideredas the lower limit of the consumed P in the AM-dust treatments (Fig. 9). They were 76 nmol L−1 at S1, 46 nmol L−1 at
S2, 98 nmol L−1 at S3, 122 nmol L−1 at S4, and 20 nmol L−1
at S5. Deducting the P concentrations in the baseline seawaters (Table 1), the minimum bioavailable P supplied bywww.biogeosciences.net/15/749/2018/

AM-dust additions was estimated to be 22 nmol L−1 at S1,−5 nmol L−1 at S2, −6 nmol L−1 at S3, 18 nmol L−1 at S4,and −20 nmol L−1 at S5. Note that the dissolved P from AM
dust was as low as 8.6 nmol L−1 in the incubation bottles,
which could not meet the demands of phytoplankton at S1and S4. The negative values implied that the P concentrations in baseline seawaters were likely enough to support thegrowth of phytoplankton.
Thus, the supply other than the theoretically dissolved
bioavailable P of 8.6 nmol L−1 induced by the AM dust
might exist. As reported in the literature, the dissolved organic phosphorus (DOP) is considered a significant portionof the dissolved P pool in oceans, especially in surface seawater (Paytan and McLaughlin, 2007). Dust input has beenreported to induce the biological mineralization of DOP to
DIP under P-deficient conditions and consequently increased
P bioavailability. DIP mineralized from DOP in the seawater would even accumulate if the demand of phytoplankton
for P was small (Mackey et al., 2012). Note that the gradual enhanced solubility of atmospheric P with the durationof exposure in seawater was also reported to contribute additional bioavailable P for phytoplankton growth (Ridame andGuieu, 2002; Mackey et al., 2012). However, no measurements of trace metals in seawater and DOP and P in the phytoplankton cells were made in our study. The lack of data on
measurements of organic P makes the interpretation rather
speculative but serves as a recommendation for future studies.

5

Conclusion

In this study, phytoplankton growth was found to be limitedby two or more nutrients (i.e., N–P or N + P + Fe) in the
NWPO and by a single nutrient (i.e., N or P) in the YS. In
the subtropical gyre of the NWPO, the addition of AM dust
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provided N–P or N + P + Fe and micro-constituents to stimulate phytoplankton growth. In comparison with the controls,
the maximum Chl a following AM-dust addition showed a
1.7- and 2.8-fold increase, while the cell abundance of largesized phytoplankton showed a 1.8- and 3.9-fold increase. As
the increased P from AM dust was negligible in comparison with the baseline P stocks, the dissolved N from AM
dust thus primarily supported phytoplankton growth in the
Kuroshio Extension. The maximum Chl a concentrations andcell abundance of large-sized phytoplankton following AMdust addition were 1.3-fold and 1.7-fold larger, respectively,
than those in the controls. In the YS, the increased P or N
by AM-dust additions primarily contributed to the growth ofphytoplankton. The Chl a concentrations in AM-dust treatments were generally higher than those in the controls, although the differences in maximum Chl a were negligible
in both groups. The increase in the cell abundance of largesized phytoplankton was < 1.7-fold compared with the controls. Comparing the difference in consumed N : P between
the AM-dust and N treatments, we found that the directly
supplied bioavailable P by AM dust in the incubated seawaters was not enough to support phytoplankton growth in the
YS, which is characterized by P limitation, and in the subtropical gyre, which is characterized by N–P co-limitation.
We suggest that there are other sources of P during the incubation, which may be explained by the enhanced solubilityof P from AM dust and/or the mineralization of DOP in theseawaters. The addition of AM dust had a potential to shift
the phytoplankton towards larger cells at all incubation stations, although it did not change the dominant taxa of phytoplankton assemblages. In general, larger positive responsesof phytoplankton induced by combined nutrients than by asingle nutrient from the AM dust were observed in our study.
This is likely related to the varying nutrient levels, community structures of phytoplankton in the baseline seawaters,
and the input of nutrients following AM-dust addition.
Our study suggests the importance of an increase inbioavailable P stock for phytoplankton growth following
AM-dust addition. This would help us better understand theeffects of dust deposition on P cycles in the ocean. In viewof the increasing anthropogenic N deposition in the NWPO
and YS due to continuously strong NOx emissions in eastern
Asia (Kim et al., 2011, 2014), the increase in bioavailable P
stock induced by dust deposition might be even more important in phytoplankton growth in the future. Moreover, further
investigations are needed to better understand the differential effects of an increase in bioavailable P stock as a resultof the atmospheric deposition on phytoplankton growth in
the coastal seas and open oceans. In terms of autotrophs, thestimulation of large-sized phytoplankton growth due to the
input of AM dust might enhance the carbon storage in the
deep ocean, as the sinking rates of large-sized cells in thewater column are higher than the pico-sized ones (Bach etal., 2012). On the other hand, the increasing anthropogenic
activities in recent years can also increase the contents ofBiogeosciences, 15, 749–765, 2018

heavy metal in the dust, which may inhibit phytoplankton
growth (Miao et al., 2005; Paytan et al., 2009). However,
the toxic effect of dust aerosol was not well reflected in ourstudy. Therefore, further studies are also needed to illustrate
the double function of dust deposition to the marine ecosystems.

Data availability. The data used in this study are available uponrequest to the corresponding author.

The Supplement related to this article is available online
at https://doi.org/10.5194/bg-15-749-2018-supplement.

Competing interests. The authors declare that they have no conflictof interest.

Acknowledgements. This work was funded by the National Natural
Science Foundation of China (NSFC; 41210008: Huiwang Gao),the Major State Basic Research Development Program of China(973 Program; 2014CB953701: Huiwang Gao), and an NSFC
and Royal Society travel grant (4141101141: Huiwang Gao andZongbo Shi).
Edited by: Manmohan Sarin
Reviewed by: four anonymous referees

References
Arrigo, K. R.: Marine microorganisms and global nutrient cycles, Nature, 437, 349–355, https://doi.org/10.1038/nature04158,
2005.
Aizawa, C., Tanimoto, M., and Jordan, R. W: Living diatom assemblages from North Pacific and Bering Sea surface waters
during summer 1999, Deep-Sea Res. Pt. II, 52, 2186–2205,
https://doi.org/10.1016/j.dsr2.2005.08.008, 2005.
Bach, L. T., Riebesell, U., Sett, S., Febiri, S., Rzepka, P., andSchulz, K. G.: An approach for particle sinking velocity measurements in the 3–400 µm size range and considerations on theeffect of temperature on sinking rates, Mar. Biol., 159, 1853–
1864, https://doi.org/10.1007/s00227-012-1945-2, 2012.
Baker, A., Kelly, S., Biswas, K., Witt, M., and Jickells, T.: Atmospheric deposition of nutrients to the Atlantic Ocean, Geophys.
Res. Lett., 30, 2296, https://doi.org/10.1029/2003GL018518,
2003.
Boyd, P. W., Jickells, T., Law, C., Blain, S., Boyle, E., Buesseler, K., Coale, K., Cullen, J., De Baar, H., and Follows, M.: Mesoscale iron enrichment experiments 1993–
2005: Synthesis and future directions, Science, 315, 612–617,
https://doi.org/10.1126/science.1131669, 2007.
Brown, M. T., Landing, W. M., and Measures, C. I.: Dissolved andparticulate Fe in the western and central North Pacific: Resultswww.biogeosciences.net/15/749/2018/

C. Zhang et al.: Phytoplankton growth response to Asian dust addition
from the 2002 IOC cruise, Geochem. Geophy. Geosy., 61, 1–20,
https://doi.org/10.1029/2004GC000893, 2005.
Burson, A., Stomp, M., Akil, L., Brussaard, C. P., and Huisman, J.: Unbalanced reduction of nutrient loads has created an offshore gradient from phosphorus to nitrogen limitation in the North Sea, Limnol. Oceanogr., 61, 869–888,
https://doi.org/10.1002/lno.10257, 2016.
Cermeno, P., Estevez-Blanco, P., Maranón, E., and Fernandez,
E.: Maximum photosynthetic efficiency of size-fractionatedphytoplankton assessed by 14 C uptake and fast repetition rate fluorometry, Limnol. Oceanogr., 50, 1438–1446,
https://doi.org/10.4319/lo.2005.50.5.1438, 2005.
Chien, C. T., Mackey, K. R., Dutkiewicz, S., Mahowald, N.
M., Prospero, J. M., and Paytan, A.: Effects of African dust
deposition on phytoplankton in the western tropical Atlantic
Ocean off Barbados, Global Biogeochem. Cy., 30, 716–734,
https://doi.org/10.1002/2015GB005334, 2016.
Coale, K. H.: Effects of iron, manganese, copper, andzinc enrichments on productivity and biomass in thesubarctic Pacific, Limnol. Oceanogr., 36, 1851–1864,
https://doi.org/10.4319/lo.1991.36.8.1851, 1991.
Coelho, F., Santos, A., Coimbra, J., Almeida, A., Cunha, A., Cleary,D., Calado, R., and Gomes, N.: Interactive effects of global climate change and pollution on marine microbes: the way ahead,
Ecol. Evol., 3, 1808–1818, https://doi.org/10.1002/ece3.565,
2013.
Duce, R., Liss, P., Merrill, J., Atlas, E., Buat-Menard, P., Hicks, B.,
Miller, J., Prospero, J., Arimoto, R., and Church, T.: The atmospheric input of trace species to the world ocean, Global Biogeochem. Cy., 5, 193–259, https://doi.org/10.1029/91GB01778,
1991.
Egge, J. K.: Are diatoms poor competitors at low phosphate concentrations?, J. Marine Syst., 16, 191–198,
https://doi.org/10.1016/S0924-7963(97)00113-9, 1998.
Franz, J., Krahmann, G., Lavik, G., Grasse, P., Dittmar, T., andRiebesell, U.: Dynamics and stoichiometry of nutrients and phytoplankton in waters influenced by the oxygen minimum zone
in the eastern tropical Pacific, Deep-Sea Res. Pt. I, 62, 20–31,
https://doi.org/10.1016/j.dsr.2011.12.004, 2012.
Fawcett, S. E. and Ward, B. B.: Phytoplankton succession and nitrogen utilization during the development ofan upwelling bloom, Mar. Ecol.-Prog. Ser., 428, 13–31,
https://doi.org/10.3354/meps09070, 2011.
Formenti, P., Schütz, L., Balkanski, Y., Desboeufs, K., Ebert,
M., Kandler, K., Petzold, A., Scheuvens, D., Weinbruch, S.,
and Zhang, D.: Recent progress in understanding physical andchemical properties of African and Asian mineral dust, Atmos. Chem. Phys., 11, 8231–8256, https://doi.org/10.5194/acp11-8231-2011, 2011.
Fu, M., Wang, Z., Li, Y., Li, R., Sun, P., Wei, X., Lin, X., and Guo,
J.: Phytoplankton biomass size structure and its regulation in theSouthern Yellow Sea (China): Seasonal variability, Cont. Shelf
Res., 29, 2178–2194, https://doi.org/10.1016/j.csr.2009.08.010,
2009.
Gao, Y., Arimoto, R., Duce, R., Lee, D., and Zhou, M.: Input of
atmospheric trace elements and mineral matter to the Yellow Sea
during the spring of a low-dust year, J. Geophys. Res.-Atmos.,97, 3767–3777, https://doi.org/10.1029/91JD02686, 1992.

www.biogeosciences.net/15/749/2018/

763

Grasshoff, K., Kremling, K., and Ehrhardt, M.: Methods of seawater
analysis, 3rd Edn., Wiley-VCH, 1999.
Guieu, C., Dulac, F., Desboeufs, K., Wagener, T., Pulido-Villena,
E., Grisoni, J.-M., Louis, F., Ridame, C., Blain, S., Brunet, C.,
Bon Nguyen, E., Tran, S., Labiadh, M., and Dominici, J.-M.:
Large clean mesocosms and simulated dust deposition: a new
methodology to investigate responses of marine oligotrophic
ecosystems to atmospheric inputs, Biogeosciences, 7, 2765–
2784, https://doi.org/10.5194/bg-7-2765-2010, 2010.
Guo, C., Yu, J., Ho, T.-Y., Wang, L., Song, S., Kong, L., and Liu, H.:
Dynamics of phytoplankton community structure in the South
China Sea in response to the East Asian aerosol input, Biogeosciences, 9, 1519–1536, https://doi.org/10.5194/bg-9-15192012, 2012.
Guo, X., Zhu, X., Wu, Q., and Huang, D.: The Kuroshio
nutrient stream and its temporal variation in the East
China Sea, J. Geophys. Res.-Oceans, 117, C01026,
https://doi.org/10.1029/2011JC007292, 2012.
Hashihama, F., Furuya, K., Kitajima, S., Takeda, S., Takemura, T.,
and Kanda, J.: Macro-scale exhaustion of surface phosphate bydinitrogen fixation in the western North Pacific, Geophys. Res.
Lett., 36, 3610, https://doi.org/10.1029/2008GL036866, 2009.
Herut, B., Zohary, T., Krom, M., Mantoura, R., Pitta, P., Psarra, S.,
Rassoulzadegan, F., Tanaka, T., and Thingstad, T.: Response of
East Mediterranean surface water to Saharan dust: On-board microcosm experiment and field observations, Deep-Sea Res. Pt.
II, 52, 3024–3040, https://doi.org/10.1016/j.dsr2.2005.09.003,
2005.
Herut, B., Rahav, E., Tsagaraki, T., Giannakourou, A., Tsiola,
A., Psarra, S., Lagaria, A., Papageorgiou, N., Mihalopoulos, N., and Theodosi, C.: The potential impact of Saharan dust and polluted aerosols on microbial populations in
the East Mediterranean Sea, an overview of a mesocosm experimental approach, Frontiers in Marine Science, 3, 226,
https://doi.org/10.3389/fmars.2016.00226, 2016.
Hsu, S. C., Liu, S. C., Arimoto, R., Shiah, F. K., Gong, G.
C., Huang, Y. T., Kao, S. J., Chen, J. P., Lin, F. J., andLin, C. Y.: Effects of acidic processing, transport history,
and dust and sea salt loadings on the dissolution of ironfrom Asian dust, J. Geophys. Res.-Atmos., 115, 1485–1490,
https://doi.org/10.1029/2009JD013442, 2010.
Jakuba, R. W., Moffett, J. W., and Dyhrman, S. T.: Evidence for thelinked biogeochemical cycling of zinc, cobalt, and phosphorus in
the western North Atlantic Ocean, Global Biogeochem. Cy., 22,1971-1976, https://doi.org/10.1029/2007GB003119, 2008.
Jickells, T., An, Z., Andersen, K. K., Baker, A., Bergametti, G., Brooks, N., Cao, J., Boyd, P., Duce, R., andHunter, K.: Global iron connections between desert dust,
ocean biogeochemistry, and climate, Science, 308, 67–71,
https://doi.org/10.1126/science.1105959, 2005.
Kanakidou, M., Duce, R. A., Prospero, J. M., Baker, A. R., BenitezNelson, C., Dentener, F. J., Hunter, K. A., Liss, P. S., Mahowald, N., and Okin, G. S.: Atmospheric fluxes of organic N
and P to the global ocean, Global Biogeochem. Cy., 26, GB3026,
https://doi.org/10.1029/2011GB004277, 2012.
Kim, I.-N., Lee, K., Gruber, N., Karl, D. M., Bullister, J. L.,
Yang, S., and Kim, T.-W.: Increasing anthropogenic nitrogen in the North Pacific Ocean, Science, 346, 1102–1106,
https://doi.org/10.1126/science.1258396, 2014.

Biogeosciences, 15, 749–765, 2018

764

C. Zhang et al.: Phytoplankton growth response to Asian dust addition

Kim, T. W., Lee, K., Najjar, R. G., Jeong, H. D., and Jeong, H.
J.: Increasing N abundance in the northwestern Pacific Ocean
due to atmospheric nitrogen deposition, Science, 334, 505–509,
https://doi.org/10.1126/science.1206583, 2011.
Kitajima, S., Furuya, K., Hashihama, F., Takeda, S., andKanda, J.: Latitudinal distribution of diazotrophs andtheir nitrogen fixation in the tropical and subtropicalwestern North Pacific, Limnol. Oceanogr., 54, 537-547,
https://doi.org/10.4319/lo.2009.54.2.0537, 2009.
Klausmeier, C. A., Litchman, E., Daufresne, T., and Levin, S. A.:
Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Nature, 429, 171–174, https://doi.org/10.1038/nature02454,
2004a.
Klausmeier, C. A., Litchman, E., and Levin, S. A.: Phytoplankton growth and stoichiometry under multiple nutrient limitation, Limnol. Oceanogr., 49, 1463–1470,
https://doi.org/10.4319/lo.2004.49.4_part_2.1463, 2004b.
Klausmeier, C. A., Litchman, E., Daufresne, T., and Levin,S.: Phytoplankton stoichiometry, Ecol. Res., 23, 479–485,
https://doi.org/10.1007/s11284-008-0470-8, 2008.
Krom, M. D., Shi, Z., Stockdale, A., Berman-Frank, I., Giannakourou, A., Herut, B., Lagaria, A., Papageorgiou, N., Pitta,
P., and Psarra, S.: Response of the Eastern Mediterranean microbial ecosystem to dust and dust affected by acid processing in the atmosphere, Frontiers in Marine Science, 3, 133,https://doi.org/10.3389/fmars.2016.00133, 2016.
Li, Q., Legendre, L., and Jiao, N.: Phytoplankton responses
to nitrogen and iron limitation in the tropical and subtropical Pacific Ocean, J. Plankton Res., 37, 306–319,
https://doi.org/10.1093/plankt/fbv008, 2015.
Liu, S., Zhang, J., Chen, S. Z., Chen, H., Hong, G., Wei, H., andWu, Q.: Inventory of nutrient compounds in the Yellow Sea,
Cont. Shelf Res., 23, 1161–1174, https://doi.org/10.1016/S02784343(03)00089-X, 2003.
Liu, Y., Zhang, T., Shi, J., Gao, H., and Yao, X.: Responsesof 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, J. Geophys. Res.-Biogeo., 118, 1763–1772,https://doi.org/10.1002/2013JG002329, 2013.
Mackey, K. R., Roberts, K., Lomas, M. W., Saito, M. A., Post,
A. F., and Paytan, A.: Enhanced solubility and ecologicalimpact of atmospheric phosphorus deposition upon extended
seawater exposure, Environ. Sci. Technol., 46, 10438–10446,
https://doi.org/10.1021/es3007996, 2012.
Maranon, E., Cermeno, P., Rodríguez, J., Zubkov, M. V., andHarris, R. P.: Scaling of phytoplankton photosynthesis andcell size in the ocean, Limnol. Oceanogr., 52, 2190–2198,
https://doi.org/10.4319/lo.2007.52.5.2190, 2007.
Maranon, E., Fernandez, A., Mourino-Carballido, B., MartinezGarcia, S., Teira, E., Cermeno, P., Choucino, P., Huete-Ortega,
M., Fernandez, E., Calvo-Diaz, A., Anxelu, X., Moran, G., Bode,A., Moreno-Ostos, E., Varela, M. M., Patey, M. D., and Achterberg, E. P: Degree of oligotrophy controls the response of microbial plankton to Saharan dust, Limnol. Oceanogr., 55, 2339–
2352, https://doi.org/10.4319/lo.2010.55.6.2339, 2010.
Maranon, E., Cermeno, P., Latasa, M., and Tadonleke, R.
D.: Temperature, resources, and phytoplankton size struc-

Biogeosciences, 15, 749–765, 2018

ture in the ocean, Limnol. Oceanogr., 57, 1266–1278,
https://doi.org/10.4319/lo.2012.57.5.1266, 2012.
Martin, J. H.: Iron still comes from above, Nature, 353, 123–123,
https://doi.org/10.1038/353123b0, 1991.
Measures, C., Cutter, G., Landing, W., and Powell, R.: Hydrographic observations during the 2002 IOC Contaminant Baseline
Survey in the western Pacific Ocean, Geochem. Geophy. Geosy.,
7, Q03M06, https://doi.org/10.1029/2004GC000855, 2006.
Meng, X., Chen, Y., Wang, B., Ma, Q., and Wang, F.: Responsesof phytoplankton community to the input of different aerosolsin the East China Sea, Geophys. Res. Lett., 43, 7081–7088,
https://doi.org/10.1002/2016GL069068, 2016.
Miao, A., Wang, W., and Philippe, J.: Comparison of Cd, Cu,
and Zn toxic effects on four marine phytoplankton by pulseamplitude-modulated fluorometry, Environ. Toxicol. Chem., 24,
2603–2611, https://doi.org/10.1897/05-009R.1, 2005.
Mills, M. M., Ridame, C., Davey, M., La Roche, J., and Geider, R. J.: Iron and phosphorus co-limit nitrogen fixation in
the eastern tropical North Atlantic, Nature, 429, 292–294,
https://doi.org/10.1038/nature02550, 2004.
Moore, C., Mills, M., Arrigo, K., Berman-Frank, I., Bopp, L., Boyd,P., Galbraith, E., Geider, R. J., Guieu, C., and Jaccard, S.: Processes and patterns of oceanic nutrient limitation, Nat. Geosci.,
6, 701–710, https://doi.org/10.1038/NGEO1765, 2013.
Moore, C. M., Mills, M. M., Langlois, R., Milne, A., Achterberg, E. P., LaRoche, J., and Geider, R. J.: Relative influence of nitrogen and phosphorous availability on phytoplankton physiology and productivity in the oligotrophic subtropical North Atlantic Ocean, Limnol. Oceanogr., 53, 291–305,
https://doi.org/10.4319/lo.2008.53.1.0291, 2008.
Noiri, Y., Kudo, I., Kiyosawa, H., Nishioka, J., and Tsuda,
A.: Influence of iron and temperature on growth, nutrient utilization ratios and phytoplankton species composition in the western subarctic Pacific Ocean during
the SEEDS experiment, Prog. Oceanogr., 64, 149–166,
https://doi.org/10.1016/j.pocean.2005.02.006, 2005.
Nishibe, Y., Takahashi, K., Shiozaki, T., Kakehi, S., Saito, H., andFuruya, K.: Size-fractionated primary production in the Kuroshio
Extension and adjacent regions in spring, J. Oceanogr., 71, 27–
40, https://doi.org/10.1007/s10872-014-0258-0, 2015.
Ooki, A. and Uematsu, M.: Chemical interactions between mineral dust particles and acid gases during Asian
dust events, J. Geophys. Res.-Atmos., 110, 1447–1454,
https://doi.org/10.1029/2004JD004737, 2005.
Paytan, A. and McLaughlin, K.: The oceanic phosphorus cycle,
Chem. Rev., 107, 563–576, https://doi.org/10.1021/cr0503613,
2007.
Paytan, A., Mackey, K. R., Chen, Y., Lima, I. D., Doney, S. C., Mahowald, N., Labiosa, R., and Post, A. F.: Toxicity of atmosphericaerosols on marine phytoplankton, P. Natl. Acad. Sci. USA, 106,4601–4605, https://doi.org/10.1073/pnas.0811486106, 2009.
Ridame, C. and Guieu, C.: Saharan input of phosphate to the oligotrophic water of the open western
Mediterranean Sea, Limnol. Oceanogr., 47, 856–869,
https://doi.org/10.4319/lo.2002.47.3.0856, 2002.
Ridame, C., Dekaezemacker, J., Guieu, C., Bonnet, S., L’Helguen,
S., and Malien, F.: Contrasted Saharan dust events in LNLC environments: impact on nutrient dynamics and primary production,www.biogeosciences.net/15/749/2018/

C. Zhang et al.: Phytoplankton growth response to Asian dust addition
Biogeosciences, 11, 4783–4800, https://doi.org/10.5194/bg-114783-2014, 2014.
Saito, M. A., Goepfert, T. J., and Ritt, J. T.: Some thoughtson the concept of colimitation: three definitions and the importance of bioavailability, Limnol. Oceanogr., 53, 276–290,
https://doi.org/10.4319/lo.2008.53.1.0276, 2008.
Sathyendranath, S., Stuart, V., Nair, A., Oka, K., Nakane,
T., Bouman, H., Forget, M. H., Maass, H., and Platt,T.: Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea, Mar. Ecol.-Prog. Ser., 383, 73–84,
https://doi.org/10.3354/meps07998, 2009.
Shao, Y., Wyrwoll, K.-H., Chappell, A., Huang, J., Lin, Z.,
McTainsh, G. H., Mikami, M., Tanaka, T. Y., Wang,
X., and Yoon, S.: Dust cycle: An emerging core themein Earth system science, Aeolian Res., 2, 181–204,
https://doi.org/10.1016/j.aeolia.2011.02.001, 2011.
Shi, J., Gao, H., Zhang, J., Tan, S., Ren, J., Liu, C., Liu,Y., and Yao, X.: Examination of causative link between aspring bloom and dry/wet deposition of Asian dust in the
Yellow Sea, China, J. Geophys. Res.-Atmos., 117, D17304,
https://doi.org/10.1029/2012JD017983, 2012.
Shi, Z., Krom, M. D., Bonneville, S., Baker, A. R., Jickells,
T. D., and Benning, L. G.: Formation of iron nanoparticles
and increase in iron reactivity in mineral dust during simulated cloud processing, Environ. Sci. Technol., 43, 6592–6596,
https://doi.org/10.1021/es901294g, 2009.
Strickland, J. D. H. and Parsons, T. R.: A practical handbook ofseawater analysis, Fisheries Research Board of Canada, Bulletin
167, Ottawa, 1972.
Sunda, W.: Feedback interactions between trace metal nutrientsand phytoplankton in the ocean, Front. Microbiol., 3, 204,https://doi.org/10.3389/fmicb.2012.00204, 2012.
Sun, J., Feng, Y., Wang, D., Song, S., Jiang, Y., Ding, C., and Wu,
Y.: Bottom-up control of phytoplankton growth in spring blooms
in Central Yellow Sea, China, Deep-Sea Res. Pt. II, 97, 61–71,
https://doi.org/10.1016/j.dsr2.2013.05.006, 2013.

www.biogeosciences.net/15/749/2018/

765

Tanaka, T., Thingstad, T., Christaki, U., Colombet, J., CornetBarthaux, V., Courties, C., Grattepanche, J.-D., Lagaria, A.,
Nedoma, J., and Oriol, L.: Lack of P-limitation of phytoplankton and heterotrophic prokaryotes in surface waters of
three anticyclonic eddies in the stratified Mediterranean Sea,
Biogeosciences, 8, 525–538, https://doi.org/10.5194/bg-8-5252011, 2011.
Twining, B. S. and Baines, S. B. The trace metal compositionof marine phytoplankton, Annu. Rev. Mar. Sci., 5, 191–215,
https://doi.org/10.1146/annurev-marine-121211-172322, 2013.
Wang, B. D., Wang, X. L., and Zhan, R. Nutrient conditions in
the Yellow Sea and the East China Sea, Estuar. Coast. Shelf
S., 58, 127–136, https://doi.org/10.1016/S0272-7714(03)000672, 2003.
Whitney, F. A.: Nutrient variability in the mixed layer of the subarctic Pacific Ocean, 1987–2010, J. Oceanogr., 67, 481–492,
https://doi.org/10.1007/s10872-011-0051-2, 2011.
Yatsu, A., Chiba, S., Yamanaka, Y., Ito, S.-I., Shimizu, Y.,
Kaeriyama, M., and Watanabe, Y.: Climate forcing and theKuroshio/Oyashio ecosystem, ICES J. Mar. Sci., 70, 922–933,
https://doi.org/10.1093/icesjms/fst084, 2013.
Zhou, M. J., Shen, Z. L., and Yu, R. C.: Responses of a coastal
phytoplankton community to increased nutrient input from the
Changjiang (Yangtze) River, Cont. Shelf Res., 28, 1483–1489,
https://doi.org/10.1016/j.csr.2007.02.009, 2008.

Biogeosciences, 15, 749–765, 2018