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RESEARCH ARTICLE
Effect of temperature on the accumulation of
marine biogenic gels in the surface microlayer
near the outlet of nuclear power plants and
adjacent areas in the Daya Bay, China
Wei-zhong Yue
1
, Cui-ci Sun
1,2
*, Ping Shi
1
, Anja Engel
3
, You-shao Wang
1,2
, Wei-Hong He
4
1State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese
Academy of Sciences, Guangzhou, China, 2Daya Bay Marine Biology Research Station, Chinese Academy
of Sciences, Shenzhen, China, 3GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany,
4South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China
*scuici@scsio.ac.cn
Abstract
The surface microlayer (SML) in marine systems is often characterized by an enrichment of
biogenic, gel-like particles, such as the polysaccharide-containing transparent exopolymer
particles (TEP) and the protein-containing Coomassie stainable particles (CSP). This study
investigated the distribution of TEP and CSP, in the SML and underlying water, as well as
their bio-physical controlling factors in Daya Bay, an area impacted by warm discharge from
two Nuclear power plants (Npp’s) and aquaculture during a research cruise in July 2014.
The SML had higher proportions of cyanobacteria and of pico-size Chl acontrast to the
underlayer water, particularly at the nearest outlet station characterized by higher tempera-
ture. Diatoms, dinoflagellates and chlorophyll awere depleted in the SML. Both CSP and
TEP abundance and total area were enriched in the SML relative to the underlying water,
with enrichment factors (EFs) of 1.5–3.4 for CSP numbers and 1.32–3.2 for TEP numbers.
Although TEP and CSP showed highest concentration in the region where high productivity
and high nutrient concertation were observed, EFs of gels and of dissolved organic carbon
(DOC) and dissolved acidic polysaccharide (>1 kDa), exhibited higher values near the out-
let of the Npp’s than in the adjacent waters. The positive relation between EF’s of gels and
temperature and the enrichment of cyanobacteria in the SML may be indicative of future
conditions in a warmer ocean, suggesting potential effects on adjusting phytoplankton com-
munity, biogenic element cycling and air-sea exchange processes.
Introduction
The sea surface microlayer (SML) is the topmost 1–1000μm of the ocean surface. In recent
years, enrichment of biogenic marine gel particles in the SML have gained increasing attention
as these gelatinous compounds may play an important role in microbial processes and carbon
cycling in the ocean as well as potentially affecting of the exchange of gas, heat and mass
between the ocean and atmosphere [1–4]. Marine gels, such as transparent exopolymer
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 1 / 25
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OPEN ACCESS
Citation: Yue W-z, Sun C-c, Shi P, Engel A, Wang
Y-s, He W-H (2018) Effect of temperature on the
accumulation of marine biogenic gels in the
surface microlayer near the outlet of nuclear power
plants and adjacent areas in the Daya Bay, China.
PLoS ONE 13(6): e0198735. https://doi.org/
10.1371/journal.pone.0198735
Editor: Wei-Chun Chin, University of California,
Merced, UNITED STATES
Received: January 5, 2018
Accepted: May 24, 2018
Published: June 11, 2018
Copyright: ©2018 Yue et al. This is an open access
article distributed under the terms of the Creative
Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in
any medium, provided the original author and
source are credited.
Data Availability Statement: All relevant data are
within the paper.
Funding: This study was supported by Special
Fund for Public Welfare Research and Capacity
Building in Guangdong Province
(2016A020222018), National Natural Science
Foundation of China (CN41106106 and No.
41430966), the National Key Research and
Development Plan (No. 2017FY100700) and China
Scholarship Council 201408440016.
particles (TEP, polysaccharidic) and Coomassie stainable particles (CSP, proteinaceous) [5,6],
are formed by exopolymers of polysaccharidic or proteinaceous composition mostly derived
from marine microorganisms during exudation, degradation and lytic processes [7–9].
Trapped by ascending bubbles, the sticky gels can be carried upward through the water col-
umn to the SML, or form from dissolved precursors directly at the air-sea interface during sur-
face wave action [10]. It has been suggested that the presence of abundant biogenic gels in the
SML can influence gas exchange between air and sea [4] and provide an important source for
marine primary organic aerosols [11,12]. Additionally, due to the sticky properties of gels,
they can aggregate both live and dead plankton, as well as mineral particles and therefore rep-
resent hotspots of microbial activity in the SML [13,14].
The major factors determining the production of biogenic gels and their precursors in the
water column include the physiological state of the phytoplankton cell and phytoplankton
community composition as well as environmental growth conditions [15–17]. Therefore, feed-
backs of phytoplankton in the surface ocean to environmental changes could be reflected in
the accumulation of marine gels in the SML [18]. Lass, Bange [19] showed that seasonal varia-
tions of abundant carbohydrate-rich polymeric material, such as TEP precursors, in the SML
were related to a combination of phytoplankton abundance and photochemical and/or micro-
bial reworking of organic matter. High TEP production has often been observed towards the
end of algal blooms or in cultures of nutrient-stressed phytoplankton [20,21]. For CSP abun-
dance, significant increase by initial NO
3
supply was observed during mesocosm experiments
[22]. In contrast to gel production in the water column, enrichments of dissolved protein frac-
tions in the SML have been inversely related to trophic status, i.e. higher enrichments were
observed in oligotrophic open ocean areas compared to more productive coastal waters [23].
CSP concentration might be influenced in the SML by the same processes as in bulk seawater
(production by or leaching from phytoplankton and bacteria; microbial degradation; photode-
gradation), but at different rates[24–26]. The different rates between SML and bulk water
might yield a different CSP turnover time and a complex pattern of enrichment in the micro-
layer[23]. While these results showed that the production of biogenic gels by phytoplankton
was tightly related to the tropic status, it is yet difficult to predict the impact of nutrients supply
on the enrichments of the gels in the SML due to co-effects on phytoplankton community
structure, in particular as we still lack information on the controlling factors for CSP formation
and accumulation in the SML and as well as in the water column.
Besides nutrients supply, temperature has been suggested to affect the production of TEP
by phytoplankton [27,28]. Thereby, the effect of elevated temperature on the production of
gels depended on the geographical temperature variability and on the interactive effects
between different environmental conditions, i.e. under moderate or cool temperature condi-
tion, the production of TEP was promoted by elevated temperature through an increasing
amount of exudates released by phytoplankton when nutrients become limiting [29–32]. But,
rising temperature could also result in an earlier onset of TEP degradation by heterotrophic
bacterial communities, which could counter act the enhanced TEP production[33]. In the low
latitude ocean characterized by higher temperature, elevated temperature is expected to result
in increased stratification of the upper water column diminishing upward nutrient supply [34,
35]. In the context of global warming, it is increasingly important to understand the depen-
dence of temperature on the accumulation of marine gels in the SML, due to the potential
importance of the biogenic gels in modifying exchange processes across the air and sea inter-
face as well as their well-known roles in microbial processes and carbon cycling.
Daya Bay (DYB) is one of the largest bays along the coast of southern China. In the past
decades, the rapid economic development and human activities in this area had a profound
influence on the environment of the bay. The marine aquaculture industry has also been one
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 2 / 25
Competing interests: The authors have declared
that no competing interests exist.
of the important industries in this area since the 1980s. Dapeng Ao, Aotou, and the north part
are mainly marine aquacultural areas. Dissolved inorganic nitrogen (DIN) increased from 1.53
to 5.40 μmol L
-1
in DYB due to anthropogenic inputs in the period from 1985 to 2004. In con-
trast, dissolved inorganic phosphorous (P) decreased from 1.12 to 0.110 μmol L
-1
, probably as
a result of ban-used detergency powder (contains phosphorous) in recent years, resulting the
average ratio of N/P increased from 1.377 in 1985 to 49.09 in 2004 [36]. Two nuclear power
plants (Npp), Daya Bay Npp (DNpp) and Ling’ao Npp (LNpp), are located on the western
coast of DYB and started up in 1994 and 2002, respectively. Cooling sea water collected from
the bottom was heated by LNpp and DNpp and taken through a common canal to discharge
into DYB. For LNpp, total rated capacity of the facility is 4000 MW and uses about 220 m
3
cooling water per second, and cooling water increased up to 9˚C by heat exchange when pass-
ing the condensers. For DNpp, the total rated capacity is 1800 MW, and the condenser circu-
lating system needs an intake and discharge flow of 95 m
3
s
-1
, with a temperature elevation of
10˚C. The formation of a seasonal thermo-cline with temperature gradient of 0.3~1.72˚Cm
-1
in DYB occurs from May to October, and is especially pronounced between July and Septem-
ber [37]. The thermal discharge has a visible influence on the thermal stratification [38]. The
difference in temperature between surface and bottom reached 5.98˚C near the output of
warm discharge, higher than a mean difference of 3.5˚C in DYB [37]. This is expected to shal-
low the mixed layer depth from 6-8m at the mouth of DYB to 2-4m at the outlet of Npp. Fur-
thermore, vertical mixing with deeper, nutrient-rich water was strongly diminished when no
strong precipitation and runoff inputs were observed in summer, after the thermocline is
established, which signals the onset of stratification [37]. Apart from the thermal discharge
from the Npp, anthropogenic nutrients inputs impose stresses on water bodies in DYB, al-
tering the phytoplankton community composition, biomass as well as the size of plankton,
especially near the aquaculture farm areas [36,39–41]. In addition, it has been shown that
autotrophic phytoneuston, i.e. organisms inhabiting the SML, in DYB is a unique community
jointly dominated by cyanobacteria and diatoms, and has a different community structure
compared to phytoplankton in the underlying bulk water [42]. Changes in the autotrophic
phytoneuston community may serve as indicators of the environmental changes in DYB, such
as increasing water temperature, global warming, and nutrient supply. Thus, it is expected that
these environmental changes influence the production and accumulation of gels in the SML as
well as in the underlying water in DYB.
The aim of this study was to investigate how properties of the SML near the outlet of
nuclear power plants in DYB, and specifically the impact of warm water discharge from Npp
affect the phytoneuston community and distribution of biogenic gels in the SML. In view of
the long-term (20-year) operation of the Npp and the accompanying increase of water temper-
ature at the Npp site, the advantage of this study compared to other ’warming experiments’
like bottle or mesocosms experiments is that we examined a natural community, which had
time to adapt to a changed environmental situation.
Materials and methods
Ethics statement
No animals were collected for these surveys, and no sites required permits for general research
during this research. This study did not involve endangered or protected species.
Sites and sampling
DYB is a semi-enclosed bay in the northwestern part of the South China Sea. It lies to the east
of the Pearl River Estuary, with an average depth of 11 m. The enclosed character of the bay
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 3 / 25
reduces the rate of water exchange with open ocean water, reinforcing the exposure to elevated
nutrient input. No large river discharges into the bay, however, there are more than ten sea-
sonal streams flowing into the bay from a short distance along the coast. Fish and shell aqua-
culture are well developed, with cage culture industry widespread in the inner of Dapeng Bay.
The East Guangdong upwelling transports cold water to DYB, and the thermal discharge from
nuclear power plant increases the thermo-cline strength during the summer from July to
August [38,43].
The cruise took place near the outlet of the thermal discharge and in the adjacent DYB area
in July 2014 (Fig 1). At this time, surface seawater temperature was the highest during the year
(range: 14.4–32.4˚C with average of 22.4˚C). Samples were collected from two sites (S1 and S2)
close to the Npp and at various distances from the hot-water site (S3-S7) to compare properties
of the SML with respect to seawater temperature. All sampling sites were located between 1.1
(S1) km and 12.2 km (S4) from the Npp. Long term monitoring data collected by the Marine
Biological Research Station (MBRS) showed that surface temperature at S1 has increased by
2–3˚C compared to S4 since the beginning of the operation of the Npp [38]. S3 was in the
Dapeng Bay, where the water is generally less affected by oceanic water inflow, because of slug-
gish water circulation. At each sampling site, salinity, temperature, and pH were measured
over the full water-column using a YSI 6600 sonde (YSI Environmental, USA).
Wind speed at 10 m above ground was retrieved from the DYB station database (http://dyb.
cern.ac.cn/) for the time of sampling, acquired using an automated Vaisala Milos 520 weather
station. The photosynthetically available radiation (PAR) and ultraviolet (UV) radiation were
determined by Vaisala Milos 520. SML samples were collected using a glass plate sampler
according to the original approach described by Harvey and Burzell [44] from a small boat.
For each sample, the glass plate was vertically inserted into the water and withdrawn at a con-
trolled rate of ~20 cm s
-1
. The sample, retained on the glass because of surface tension, was
removed by a Teflon wiper. Samples were collected into acid cleaned (HCl, 10%) and Milli-Q
washed glass bottles. Prior to sampling, both glass plate and wiper were washed with HCl
(10%) and intensively rinsed with Milli-Q water. Between samplings, both instruments were
copiously rinsed with seawater to minimize their contamination with alien material while han-
dling or transporting the devices. Samples were collected as far upwind of the boat as possible
and away from the path taken by the small boat to avoid contamination.
The apparent thickness (d) of the layer sampled with the glass plate can be determined as
follows:
d¼V=ðAnÞ ð1Þ
where Vis the SML volume collected, Ais the sampling area of the glass plate and nis the
number of dips. We will use d(μm) as an operational estimate for the thickness of the SML. At
the same stations, after sampling the SML, samples from subsurface layer (SSL) were collected
with a Niskin water sampler at 0.5 m below the surface, respectively. The SML thickness deter-
mined from a total of n = 7 samples, ranged from 41–58μm, with a mean value of 44.85
±5.93 μm. This value is consistent with the previous observations with a glass plate at the same
withdraw rate [45].
Results from the SML samples were compared to those of underlying water and expressed
as enrichment factors (EF), defined as:
EF ¼ ðCÞSML=ðCÞSSW ð2Þ
Where (C) is the concentration of a given parameter in the SML or SSW water, respectively
[46]. Enrichment of a component is generally indicated by EF>1, depletion by EF<1.
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 4 / 25
Fig 1. Sampling stations and surface temperature distribution in Daya Bay (DNpp, Daya Bay Nuclear Power Plant; LNpp, Lingao Nuclear Power Plant,
MBRS, Daya Bay Marine Biology Research Station).
https://doi.org/10.1371/journal.pone.0198735.g001
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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Biological and chemical measurements
Inorganic nutrients and phytoplankton community structure. A 250-ml aliquot water
was gently filtered (<100 mbar) through 20 μm nylon membrane (Millipore), 2.0 μm and
0.2 μm polycarbonate membrane filters (Millipore) using a serial filtration unit and fraction-
ated into pico- (<2.0 μm), nano- (2.0–20.0 μm) and micro-phytoplankton (>20 μm) size frac-
tions [47]. Chl aconcentration was determined using fluorescence method after extraction in
90% acetone for 24 h. The filtrates were used for dissolved nutrient analysis, including DIN,
(the total of nitrate, nitrite and ammonia) and DIP. Nutrient analysis was done in triplicate fol-
lowing Strickland and Parsons [48].
For phytoplankton counting, samples were fixed with pre-filtered paraformaldehyde (0.5%
final concentration) for 30 min and flash frozen in liquid nitrogen, and stored at -80˚C until
analysis. Three major groups of phytoplankton, cyanobacterial (mainly Synechococcus spp.
populations), and eukaryotic phytoplankton of pico-size were discriminated and enumerated
based on their auto-fluorescence properties using a flow cytometer (Becton & Dickinson
FACSCalibur) equipped with a laser emitting at 488 nm. Synechococcus spp. populations were
distinguished principally by their orange fluorescence and separated from the distributions of
other populations in the plot of red vs blue florescence. Picoeukaryotes always showed the larg-
est red fluorescence and slide scatter. Cell counts were analyzed using BD CellQuest Pro-
Software.
Samples for characterizing the microphytoplankton community composition were stored
using 10% formalin (final conc. 1%). The concentrated sample was examined by inverted light
microscopy at magnifications of 400x, after settling 25 mL in Utermo¨hl chambers for 24 h.
Diatoms, dinoflagellates and cyanobacteria were enumerated in fields of view with 0.5 mm
diameter.
Total organic carbon (TOC), dissolved organic carbon (DOC) and particulate organic
carbon (POC). Samples for TOC and DOC (20 mL) were collected in combusted glass
ampoules, DOC after filtration through combusted GF/F filters (8 h, 500˚C). Samples were
acidified with 80 μL of 85% phosphoric acid, heat sealed immediately, and stored at 4˚C in the
dark until analysis. DOC and TOC samples were analyzed by applying the high-temperature
catalytic oxidation method (TOC-VCSH, Shimadzu) modified from Sugimura and Suzuki
(1988). Potassium phthalate standard calibration was conducted over the range 0 to 250 μmol
C L
-1
. The blank of the analytical system was between 5 and 10 μmol C L
-1
and the standard
deviation was less than 3% of the mean of triplicate measurements. Particulate organic carbon
(POC) was determined as the difference between TOC and DOC.
Gel particles. Total area, particle numbers and equivalent spherical diameter (dp) of gel
particles were determined by microscopy [49]. 2 to 10 mL were gently filtered (<150mbar)
onto 25mm Nuclepore membrane filters (0.4 μm pore size, Whatman Ltd.), stained with 1 mL
Alcian Blue solution for TEP and 1mL Coomassie Brilliant Blue G (CBBG) working solution
for CSP. Excessive dye was removed by rinsing the filter with Milli-Q water. Blank filters for
gel particles were taken using Milli-Q water. Filters were transferred onto Cytoclear slides and
stored at -20˚C until microscopically analysis. For each filter, thirty images were randomly
taken at ×200 magnification with a light microscope. An image-analysis software (Image J, US
National Institutes of Health) was used to analyze particle numbers and area.
The size-frequency distribution of TEP and CSP gels was described by:
dN=dðdpÞ ¼ kdd
pð3Þ
where dNis the number of particles per unit water volume in the size range d
p
to(dp +d(d
p
))
[50]. The factor kis a constant that depends on the total number of particles per volume, and δ
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 6 / 25
(δ<0) describes the spectral slope of the size distribution. The less negative is δ, the greater is
the fraction of larger gels. Both δand kwere derived from regressions of log[dN/d(d
p
)] versus
log[d
p
].
For fractal scaling of particle size distribution, three linear regions with different slopes can
be determined in accordance with the three collision mechanisms, Brownian motion, fluid
shear and differential sedimentation [51]. Brownian motion controls small particles ranging
from 0.1 to 2 μm. For the size of 2–60 μm, fluid shear is considered to dominate, and differen-
tial sedimentation becomes dominant for particles larger than 60 μm [52]. If larger gels-parti-
cle aggregates are denser than seawater due to higher proportion of attached solid particles in
the coastal area, these larger particles would be expected to settle out of the SML, consequently
reducing their abundance in the SML [16]. Thus, in this study, slope for all size gel particles
was determined only for the size of 2–60μm ESD.
Concentrations of TEP
color
(μg Gum Xanthan equivalents (Xeq.) L
-1
) were measured using
the method of Passow and Alldredge[53]. Triplicate 40 ml samples were vacuum filtered
(<200 mbar) onto 25 mm diameter, 0.4 μm polycarbonate filters (Millipore). Filters were
stained for <5 s with 0.5 mL of 0.02% Alcian Blue 8GX (Amresco) in 0.06% acetic acid (pH
2.5) and then rinsed with 2.0 mL of deionized water. Alcian Blue-stained material was
extracted from the filters with 6 mL of 80% sulfuric acid for 2 h on an oscillator. Absorbance of
the supernatant fluid was measured spectrophotometrically at 787 nm. Alcian Blue absorption
was calibrated using a Xanthan Gum solution (SIGMA) that was processed by tissue grinder
and measured by weight.
Dissolved acidic polysaccharides (DAPS) were measured using an Alcian Blue staining
method [54]. 20 ml samples were filtered through 0.2 μm pore-size syringe filter containing a
surfactant-free cellulose acetate (SFCA) membrane. The filtrate was collected into sterile poly-
ethylene centrifuge tubes, preserved with 0.2 mL formalin and stored refrigerated (4˚C) until
analysis. Alcian Blue can precipitate with salts. In order to remove inorganic salts interferences
([53,54]), duplicate samples after shaking were desalinated by dialysis tubing with a molecular
weight cut-off of 1000 Da (Spectra/Por 7 regenerated cellulose, Spectrum Laboratories) for
approximately 20 h. A few drops of chloroform were added to the water bath to inhibit micro-
bial growth. After dialysis, 5 mL of sample were filled into a tube and reacted with 1 mL of
Alcian Blue (0.02% [w/v] in 0.06% acetic acid [v/v] [55], and adjusted to pH 2.5 with acetic
acid. The mixture was vigorously mixed and left to stand for 5 min before mixing once more.
The entire 6 mL were placed in a 10-mL syringe and filtered through a 0.2-μm-pore-size SFCA
filter (Nalgene), and the last 1 mL of filtrate was measured at 610 nm against an ultra-high-
purity (UHP) water blank using a spectrophotometer (Shimadzu UV 1700). The Alcian Blue
side chains react with the acidic groups of polysaccharides yielding an insoluble non-ionic pig-
ment, which is retained on the filter. The absorbance of the filtrate is inversely proportional to
the concentration of DAPS in the sample. Two replicate samples were analyzed. It should be
mentioned that only high molecular weight (>1kDa) DAPS can be determined with this
method. DOM <1kDa will pass the dialysis membrane.
Data analysis
Analysis of variance or Student’s t-test was conducted on the data that met the assumptions of
normality and equality of variance. Data that did not meet these criteria were log (n + 1)-trans-
formed before analyses, or nonparametric tests were carried out on the ranks. Nonparametric
statistics (Kolmogorov-Smirnov test) was used to compare gels spatial–temporal differences.
Tukey’s honestly significant difference (Tukey HSD) test was used to compare the concentra-
tion of various substances at each station. Pearson product moment correlation analyze was
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 7 / 25
used to examine the relationship among gels concentration and relevant environmental
parameters. Principal component analysis (PCA) was employed to identify the key variables
with the highest influence on parameters characteristics, directly on a correlation matrix. Sta-
tistical calculations were conducted using Origin9.0 (Origin Lab Corporation, USA).
Results
Physical parameters
Fig 1 showed the warm plume released from the LNpp and DNpp. S1 was the nearest station to
the thermal outlet from Nuclear Power Plant during this cruise. Thus, the surface temperature
at this site was the highest, and elevated about 3.0˚C above lowest water temperature observed
at S7 as shown in Fig 1 and Table 1. Moreover, the warm discharge from Npp resulted in the
strongest stratification in temperature at S1 (Fig 2), where the difference of temperature
between surface and bottom was 5.5˚C. Temperature at S1 was relatively uniform in the upper 2
m, whereas the depth of thermocline at the other sites varied between 4 and 8m (Fig 2). This
indicated that the thermocline in strength and depth varied spatially as a function of thermal
discharge from Npp. The Southeast Asian southwesterly monsoon winds prevail with lower
speed from May to September. Low wind speeds were recorded between 2.5 and 3.6 ms
-1
during
this cruise. The surface salinity ranged between 29.89 and 32.94 with the lowest salinity being
observed at S3 (Table 1). During the cruise, the photosynthetically available radiation ranged
from 740.5 to 1916.9 μmol m
-2
s
-1
, and the maxima of UV radiation was 54.6 W m
-2
.
Phytoplankton structure and nutrients
Total concentrations of Chl avaried between 1.78 and 4.19 μg L
-1
in the SML (Fig 3A), and
between 2.74 and 6.22 μg L
-1
in the SSL (Fig 3B), respectively. In general, highest Chl aconcen-
trations were observed at and close to the fish farming stations, (S2 and S3). Chl aconcentra-
tion was dominated by nano-phytoplankton with an averaged contribution of 43%. Spatial
variability of Chl asize fractions in the SML showed the highest contribution of pico-phyto-
plankton of 48% at S1 and the lowest contribution of 21% at S4, respectively (Fig 4A).
Although there was depletion of total Chl aconcentration, pico-phytoplankton were slightly
accumulated in the SML (Fig 3C).
Abundances of picophytoplankton measured by flow cytometry are shown in Fig 4.Syne-
chococcus spp. dominated bulk pico-phytoplankton abundance, whereas Prochlorococcus pop-
ulations were not detected in this study. Pico-phytoplankton abundances varied between
1.19×10
5
and 2.48×10
5
10mL
-1
for Synechococcus spp. (Fig 4A) and between0.05×10
5
and
0.09×10
5
mL
-1
for picoeukaryotes (Fig 4B). Highest abundance for Synechococcus spp. was
observed at S3 for SSL samples and at S5 for the SML samples, respectively. The enrichment of
Table 1. Hydrographic conditions in Daya Bay.
Station Geographic
coordinates
Temperature(˚C) Salinity (‰) Depth(m)
Surface Bottom Surface Bottom
S1 114.5737˚ E, 22.6040˚ N 32.4 26.9 30.62 32.84 11.5
S2 114.5543˚ E, 22.5891˚ N 31.2 26.5 30.53 32.85 9.3
S3 114.5174˚ E, 22.5700˚ N 29.9 26.3 29.89 30.03 7.2
S4 114.6391˚ E, 22.5391˚ N 29.3 25.1 30.16 33.02 18.6
S5 114.5625˚ E, 22.5654˚ N 30.0 25.3 30.22 32.83 10.2
S6 114.6217˚ E, 22.6050˚ N 29.9 25.5 30.17 32.87 16.3
S7 114.6508˚ E, 22.6100˚ N 29.2 25.3 30.55 32.93 13.6
https://doi.org/10.1371/journal.pone.0198735.t001
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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pico-phytoplankton abundance differed spatially, with higher EF at the stations near the outlet
of warm discharge from Npp (S1:EF
Synechococcus spp.
= 1.35, EF
pico-euk
= 1.46) but depleted at S3
(EF
Synechococcus spp.
= 0.68, EF
pico-euk
= 0.83).
Fig 2. Vertical distribution of temperature at S1, S2 and S4.
https://doi.org/10.1371/journal.pone.0198735.g002
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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Fig 3. Size fractionation of Chl ain Daya Bay and enrichment factors. (A) Size fractionation of Chl ain the SML;
(B) Size fractionation of Chl ain the SSL; (C) Enrichment factors of different size of Chl a.
https://doi.org/10.1371/journal.pone.0198735.g003
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 10 / 25
Fig 4. Synechococcus spp. and picoeukaryotes abundance in the SMLand SSL in Daya Bay determined by flow cytometer.
(a) Synechococcus spp. abundance; (b) picoeukaryotes abundance.
https://doi.org/10.1371/journal.pone.0198735.g004
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 11 / 25
Phytoplankton abundance and community composition as determined by microscopy are
shown in Fig 5A–5C. Phytoplankton cell densities ranged between 5.26×10
3
to 12.1×10
3
cells
L
-1
in the SSL with the mean of 6.86±2.38×10
3
cells L
-1
. Diatoms, the dominant phytoplankton
group, contributed 81.9% to total cell abundances in the SSL. The common dominant taxa
included Rhizosolenia delicatula,Rhizosolenia fragilissima, and Pseudo-nitzschia pungens.
Dinoflagellates, dominated by Scrippsiella trochoidea, represented 16.0% of total abundances;
Trichodesmium, a widespread marine cyanobacterium with high nitrogen fixation properties
was observed at S1, S2, S3 and S5. Clear differences were observed for the algal community
between SML and underlying water determined in this study. Diatoms and dinoflagellates
were clearly depleted in all SML samples (mean of EF
Diatoms
= 0.56±0.07 and mean of EF
Dino-
flagellates
= 0.69±0.09). In contrast to the SSL, the SML had higher abundance and proportions
of Trichodesmium spp., representing on average 12% of total phytoneuston abundance. Den-
sity of Trichodesmium spp.in the SML spatially varied from 36 to 1070 filaments L
−1
, with
higher density at S1, S2 and S3 (Fig 5C).
Concentration of DIN was generally below 10 μmol L
-1
in the SML and SSW, except for sta-
tion S7 where DIN was 10.36 μmol L
-1
in the SML (Table 2). The spatial distribution revealed
that DIN concentrations were higher in the mouth of DYB and in the region far from the Npp
discharge (S6 and S7). DIP concentration was on average 0.18 and 0.14 μmol L
-1
in the SML
and SSL, respectively. Ratios of DIN and DIP varied spatially from 20.7 to 54.7. Relatively low
DIN/DIP ratios of about 20 were observed at S1 and S2. Nutrients were enriched in the SML
on all stations, with EF’s ranging from 1.22 to 1.58 for DIP and from 1.24 to 1.52 for DIN
(Table 2).
Organic matter accumulation in the SML
Fig 6 shows the biogenic gels concentration in the SML and SSL. CSP abundance ranged from
84.9×10
6
to 379×10
6
L
-1
in the SML and from 65.0 ×10
6
to 181×10
6
L
-1
in the SSL. CSP num-
bers and total areas at S4, S6 and S7 were significant lower than those of the other stations
(non-parameters t-test, p <0.05). TEP abundance was clearly lower than CSP abundance on
all stations, with a mean value of 95.9±60.7 ×10
6
L
-1
in the SML and 47.9±30.3×10
6
L
-1
in the
SSL. Spatial variability of TEP abundance was similar to CSP abundance and yielded the high-
est value at S3 in the Dapeng bay. Abundance or total area of gels in the SML was significantly
related to the respective concentration in the SSL (p<0.01). Thus, a similar pattern of spatial
variability was observed for EF’s for abundance and total area of gel particles. EF’s varied from
1.5 to 3.4 for CSP numbers and from 1.32 to 3.2 for TEP numbers, respectively (Fig 7). A sig-
nificant correlation was observed between the enrichment of microgels and temperature
(p<0.05).
The slope of the particles size spectrum could be described with the power law function
given in Eq 3. The abundance in CSP and TEP in the SML followed the standard pattern of
decrease in abundance with increasing particle size (r
2TEP
= 0.99±0.01; r
2CSP
= 0.96±0.02). The
parameter δdescribes the slope of the particles size spectra 2–60. For TEP, the slope varied
from -2.49 to -2.19 (mean value: -2.30, SD: 0.11) for particles in the SML. The slope of CSP
ranged from -2.18 to -1.83 (mean value:-1.95, SD: 0.12) in the SML. Lower values of slopes
indicate relatively higher abundance of smaller particles. The slope of gels at S1 in the SML was
significantly different from the other stations (p<0.05). The size distribution of gels with stee-
pest slope for both CSP (δ= -2.18) and TEP (δ= -2.49) in the SML at S1 indicated a relatively
higher abundance of smaller gels as shown in Fig 8, whereas maximum PSD slope was consis-
tent with relatively more and larger-sized gels at the S4 where temperature was not affected
totally by the Npp thermal discharge.
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 12 / 25
Fig 5. Phytoplankton abundance in the SML and SSL determined by light microscopy in Daya Bay. (a) Diatom
abundance (cell L
-1
); (b) Dinoflagellate abundance (cell L
-1
); (c) Trichodesmium spp. abundance (filament L
-1
).
https://doi.org/10.1371/journal.pone.0198735.g005
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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DOC concentrations ranged between 124.9 and 183.6 μmol L
-1
and from 133.3 to
178.8 μmol L
-1
in the SML and SSL, respectively (Table 3). For DOC at all stations, no enrich-
ment was observed except for S1, showing a slight enrichment. Highest POC concentration
water occurred at S3 both in the SSL and SML. In contrast to DOC, POC concentration was
strongly enriched in the SML, at all stations. The average of DAPS concentrations were 2786.2
±328.1μg L
−1
and 3017.8±288.8μg L
−1
in the SML and SSL, respectively. A positive relationship
was observed between DAPS and TEP
color
concentrations (r
2
= 0.678, p = 0.027). Similar to
DOC, a relative enrichment of DAPS was more pronounced in SML of S1 (EFs = 1.26) than at
other stations (Fig 7).
Principal components analysis (PCA) for gels and environmental
parameters
The relationships among the parameters, and spatial changes of biochemical parameters were
further distinguished by PCA (Fig 9). The distribution of gel number was generally consistent
with that of gel area, thus number was used in PCA. PCA showed that the first and the second
principal components accounted for 44.75 and 31.85% of the total variability, respectively.
Variability along the first axis was mainly explained by Chl-aconcentration in the nano-size
range, by diatom abundance as well as by CSP and TEP concentrations. It indicated that gel
concentrations were related to the biomass. The second principal component (PC2), was asso-
ciated with variables such as CSP, temperature, phosphate pico-Chla and cyanobacteria
(mainly Trichodesmium spp.). It meant that the elevated temperature favored cyanobacteria
and pico-phytoplankton growth. Among the investigated environmental variables, tempera-
ture, pico-size Chl aand cyanobacteria exhibited positive correlations with biogenic gels
Table 2. Nutrients concentration in Daya Bay.
Stations DIP
[μmol L
-1
]
DIN
[μmol L
-1
]
DIN/DIP
S1 SML 0.22 4.84 21.8
SSL 0.18 3.77 20.7
EF 1.22 1.29
S2 SML 0.22 5.73 25.5
SSL 0.17 3.76 21.8
EF 1.30 1.52
S3 SML 0.15 5.19 34.9
SSL 0.12 3.44 29.5
EF 1.27 1.51
S4 SML 0.15 7.05 45.6
SSL 0.10 5.36 54.7
EF 1.58 1.32
S5 SML 0.16 4.41 27.5
SSL 0.12 3.56 29.0
EF 1.31 1.24
S6 SML 0.14 7.31 53.3
SSL 0.10 4.99 48.3
EF 1.33 1.47
S7 SML 0.22 10.36 46.7
SSL 0.17 7.60 44.1
EF 1.29 1.36
https://doi.org/10.1371/journal.pone.0198735.t002
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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numbers in the SML. The samples could be divided into three subgroups: one group influ-
enced by the warm discharge from Npp, with relatively higher temperature, phosphorus, high
concentration of picoplankton Chl aand abundant gels in the SML; one group far from Npp
was negatively related to PC1 and PC2 axes, with relative high DIN concentration. Samples
from S3 distributed in the region of larger positive values of PC1, with relatively highest Chl a
concentration in the micro- and nano-size classes.
Discussion
The SML is a highly dynamic and heterogeneous layer with strong atmospheric influences.
Wind speed is one of the primary factors that determines the enrichment and fate of particu-
late material in the SML [56–58]. Wind speed <5 ms
-1
has little influence on the disruption of
SML, due to the lack of near-surface mixing associated with a smooth surface without waves
Fig 6. Abundance and total area distributions for TEP and CSP in the SML and SSL in Daya Bay. (a) CSP area and
abundance; (b) TEP area and abundance.
https://doi.org/10.1371/journal.pone.0198735.g006
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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[57,59]. In DYB, the SML is prone to formation of gelatinous films in summer, when wind
speed is typically <5 m s
-1
[60]. In this study, TEP and CSP were ubiquitous in the SML with
EFs of 1.32–3.4. This is consistent with previous studies demonstrating that the SML is
enriched in biogenic microgels [10,16]. The wind speed during sampling was between 2.5–3.6
ms
-1
supporting the accumulation of gels in the SML. Therefore, the effect of wind speed is not
addressed in more detail in this study.
Data collected in this study showed that all biological and chemical components deter-
mined in the SML exhibited a close correlation with those in the underlying water, indicating
that the SML reflects the ecosystem dynamics of the subsurface seawater system[16].
Many studies including biogeographic surveys, community-level experiments and single-
species experiments indicate that average cell size of phytoplankton tend to become smaller in
warmer waters [61–63]. The effects of temperature on size can be attributed both to direct tem-
perature effects and to indirect effects mediated by nutrient supply [64,65]. Stratification in
DYB was observed from May to October with the mixing layer of 4-5m before onset of
Fig 7. Enrichment factors for organic matter in the SML in Daya Bay.
https://doi.org/10.1371/journal.pone.0198735.g007
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 16 / 25
operation of the first Npp in 1980. It has been suggested that the warm discharge from Npp
increases and prolongs the stratification at DYB [66]. During this study, temperature at the
outlet of warm discharge decreased more rapidly with depth at 2m than waters farther away
from the NPP. This suggested that the warm water discharge changed the vertical mixing
regime in the proximity of the Npp. Furthermore, the lower level of DIN in the SML and SSL
at S1 indicated that the increase in stratification could limit the nutrients vertical exchange
across the pycnocline, or that nutrients were consumed more rapidly at higher temperature.
This reduction in nutrient concentration may additionally shift community size to smaller
Fig 8. Size-frequency distribution of gel particles in the SML at S1 and S4.
https://doi.org/10.1371/journal.pone.0198735.g008
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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species under warmer conditions [61,67]. It has also been reported that low nutrient concen-
trations at higher temperatures affect the distribution diatom to a greater extent than small
phytoplankton, such as picocyanobacteria [68]. Our results showed that the proportion of
pico-Chl ato total Chl avaried spatially, with the highest contribution of pico-sized phyto-
plankton observed in the SML at S1 and S2, characterized by higher temperature, stronger
stratification and low inorganic nitrogen concentrations relative to the samples collected far
from the outlet of warm discharge. The observation of relative high enrichments of small pico-
phytoplankton cells in the present study is similar with the findings of Wurl et al who reported
increased abundance of total prokaryotic cells and picophytoplankton in slicks [4]. The reduc-
tion in plankton cell size could arguably result in a decrease of aggregate formation [69,70],
since coagulation rates, among others, are a function of particle number and size [35]. Thus,
changes in plankton size could also affect the buoyancy and hence, potentially increasing their
retention time and abundance of TEP in the surface.
Table 3. Concentration of various organic components.
Stations TEP
color
(μg Xeq L
−1
) DAPS (μg L
−1
) DOC (μmol L
−1
) POC (μmol L
−1
)
SML SSL SML SSL SML SSL SML SSL
S1 469.6±22.6 223.4±25.7 3131.7±272.5 2482.2±253.7 160.6±5.3 137.2±5.8 44.2 22.1
S2 548.5±51.7 324.2±30.1 3226.4±332.7 2947.6±299.0 178.8±7.7 163.3±7.8 48.6 26.5
S3 611.6±53.9 459.7±43.8 3397.8±364.1 3283.6±309.6 172.6±8.2 183.6±9.6 79.9 42.6
S4 270.1±22.4 191.6±20.5 2701.4±252.8 2531.8±247.9 133.3±7.3 124.9±5.7 28.4 19.9
S5 620.0±53.4 387.5±34.2 3189.9±306.9 3127.3±311.0 165.2±6.9 162.0±7.6 35.4 21.2
S6 488.4±45.2 319.2±31.6 2824.6±293.5 2591.4±244.3 167.9±7.2 154.1±8.9 34.2 23.7
S7 434.4±33.9 301.7±28.4 2653.6±255.1 2539.3±273.9 148.3±6.7 141.9±9.3 35.6 22.7
https://doi.org/10.1371/journal.pone.0198735.t003
Fig 9. Ordination diagram displaying the first and second axes of principal components analysis (PCA). Loadings
of the environmental and biological variables (DIN, dissolved inorganic nitrogen; P, dissolved inorganic phosphorus;
Dino, Dinoflagellate; Cyano, cyanobacteria(mainly Trichodesmium spp.); Pico, Pico-size Chla; Nano, Pico-size Chla;
Micro, Micro-size Chla) are displayed as blue line; the scheme for temporal variation of water parameters of samples
depending on the scores of the first two principal components.
https://doi.org/10.1371/journal.pone.0198735.g009
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
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EPS-induced DOC self-assembly and gel formation near the warm discharge can be stimu-
lated via enhancement of hydrophobic interactions with temperature [71]. It has been sug-
gested that temperature-induced conformational changes of amphiphilic polymers produce
increased hydrophobic contact area and a higher probability of interchain bonding [71,72]. In
this study, the small size (0.4–2 μm) CSP and TEP contributed the majority of total microgels
abundance in the SML at S1. It is in accordance with the observation that the equilibrium
microgel size decreased with increased temperature [73]. In addition, strong pycnoclines due
to warm discharge from Npp may slow-down settling speeds of aggregates [74], eventually
supporting that biogenic gels particles experiences longer residence time in the upper water
column at the Npp outlet. Also, the higher temperature may increase DOM, specifically carbo-
hydrate exudation, leading to higher gel particles precursors [26]. Furthermore, higher tem-
perature can increase the degradation rate of DOM and gel particles by heterotrophs [33].
Therefore, smaller gels observed at the vicinity of the Npp during this study may also indicate
to enhanced heterotrophic degradation of larger gel particles.
Synechococcus spp. dominated pico-phytoplankton abundance during this study, corrobo-
rating previous findings that cynaobacteria like Lyngbya,Oscillatoria and Synechococcus spp.,
are important contributors to the total primary productivity in the SML in DYB [42]. Apart
from Synechococcus spp., Trichodesmium spp. were observed only at the sites of S1, S2, S3 and
S5, where the temperature was influenced by warm discharge. Trichodesmium, N-fixing cyano-
bacteria, have optimal growing conditions in warm, calm and stratified water [75,76]. Thus,
the environment conditions in DYB, characterized with persistent stratification and lower N:P
ratios as well as high temperature during summer may favor cyanobacterial growth. Enrich-
ment of Synechococcus spp. in the SML can also be attributed to an efficient adaption to UV-B
stress by modifying the cellular photosystem [77,78]. Changes in species composition may
influence gel type and production[29,79]. However, relatively little is known about exudation
and gel particles formation in cyanobacteria communities compared to diatoms [80]. High
light intensity was shown to increase the exudation of DON and DOC in cultures of Nodularia
spumigena, with maximum exudates increase during the light period [81]. Additionally, obser-
vations of a pure culture of Synechococcus bacillaris by Cisternas-Novoa, Lee [79] showed that
this cyanobacteria formed aggregates enriched in CSP. In our study, PCA indicated that gel
numbers in the SML were positively correlated with temperature, cyanobacteria (mainly Tri-
chodesmium spp.) and pico-Chl a. It is therefore speculated that the spatial distribution of gels
in the SML of DYB can partly be explained by the presence of diazotrophic cyanobacteria and
potentially increased nitrogen and carbon exudation stimulated by higher temperature.
Although similar spatial pattern in abundance and total area were observed for CSP and TEP,
these two type of gels showed different characteristics in DYB as concentrations in the SML
were significantly higher for CSP than for TEP. Also, the slope of TEP was steeper than that of
CSP, indicating more small TEP relative to CSP. Higher abundance of CSP compared to TEP
has been observed previously at other marine sites [16,82] and have been explained by CSP
being less involved in aggregate formation and sinking out of the SML [16,79].
It has been shown that high PAR and UVR could cleave DOC polymers, inhibit their spon-
taneous assembly, and/or disperse assembled microgels in SML [83], potentially affecting poly-
mer dynamics in DYB. However, Mycosporine-like amino acids (MAAs) released from
phytoplankton can be enriched in SML and exhibits an exponential rise in absorption in the
UV as a protection against UV in the SML. In addition, particulate MAAs also can absorb UV
radiation although in a narrow spectral band [84]. CSP may contain aromatic amino acids
which can absorb UV light to different degrees [85]. No assessment was made, however, of
whether CSP or amino acids accumulation in the SML could be a mechanism for UV attenua-
tion due to the aromatic amino-acids present in the CSP.
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 19 / 25
Conclusion
Our study showed that human influences, specifically seawater warming and eutrophication,
affected the biogenic composition of the SML in DYB. Maximum concentration of gel particles
and organic matter were observed in the Dapeng with high productivity, where water quality
was impacted by the aquaculture and land nutrients load. Near the outlet of Npp, seawater
experienced increased temperatures, more intense of thermal stratification. These environ-
mental drivers combined with high UV radiation had substantial effects on phytoplankton
species composition and biomass, especially favoring cyanobacteria over other phytoneuston
and increasing contribution of pico phytoplankton to the total biomass in the SML. Inversely,
diatom and dinoflagellate were depleted in the SML. Accumulation of gel particles differed
spatially. Higher enrichment of gel particles and dissolved organic matter in the SML near the
warm discharge outlet, and positive relationship between CSP and temperature and cyanobac-
teria suggested that gel particles in the SML were related to the increased temperature and cou-
pled with the variation of phytoplankton activities, thus potentially influencing the
biogeochemical cycling of nitrogen between the ocean and the atmosphere.
Reduction of gel size could increase the buoyancy and hence retention time of gels in surface
waters[86], potentially increasing their abundance in the SML. A strong enrichment of TEP and
CSP in submicron sea spray aerosol under field conditions has been observed [87]. Therefore,
in the context of global warming, the decrease in gel size together with the increase in gel abun-
dance in SML may favor organic aerosol formations, potentially changing the organic composi-
tion in the submicron sea spray aerosol. In addition, it seems more likely that in a warming
scenario the impact of the SML on gas exchange may be higher since organics were in general
more enriched at higher temperature. To better understand the role of temperature on the accu-
mulation of microgels in the SML and the consequent potential for matter exchange across sea-
air interface, future studies may need to address the relationship of microgels with other factors
including bacterial effect, virus, and physical forcing, such as UV radiation and wind speeds.
These are also important steps necessary to describe the effect of microgels on the process across
sea-air interface in the context of higher temperature eventually.
Author Contributions
Conceptualization: Wei-zhong Yue, Cui-ci Sun, Anja Engel, You-shao Wang.
Data curation: Wei-zhong Yue, Cui-ci Sun, You-shao Wang.
Formal analysis: Wei-zhong Yue, Cui-ci Sun, Ping Shi, Anja Engel, You-shao Wang.
Funding acquisition: Cui-ci Sun, Ping Shi, You-shao Wang.
Investigation: Wei-zhong Yue, Cui-ci Sun, Ping Shi, You-shao Wang, Wei-Hong He.
Methodology: Wei-zhong Yue, Cui-ci Sun, Anja Engel.
Project administration: Cui-ci Sun, Ping Shi, You-shao Wang, Wei-Hong He.
Resources: Wei-zhong Yue, Cui-ci Sun.
Software: Wei-zhong Yue, Cui-ci Sun.
Supervision: Wei-zhong Yue, Cui-ci Sun, Ping Shi, Anja Engel, You-shao Wang.
Validation: Wei-zhong Yue, Cui-ci Sun, Anja Engel, You-shao Wang.
Visualization: Wei-zhong Yue, Cui-ci Sun, Anja Engel, You-shao Wang.
Writing – original draft: Wei-zhong Yue, Cui-ci Sun.
The accumulation of marine biogenic gels in the surface microlayer in the Daya Bay, China
PLOS ONE | https://doi.org/10.1371/journal.pone.0198735 June 11, 2018 20 / 25
Writing – review & editing: Wei-zhong Yue, Cui-ci Sun, Ping Shi, Anja Engel, You-shao
Wang, Wei-Hong He.
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